Commentary: Oxidative stress as a cost of reproduction: beyond the simplistic trade-off model

Abstract

A commentary onOxidative stress as a cost of reproduction: beyond the simplistic trade-off model by Speakman, J. R., and Garratt, M. (2014). Bioessays 36, 93-106. doi: 10.1002/bies.201300108 Current theory proposes that life history traits cannot be simultaneously maximized because there are costs paid in the currency of fitness when a change in one trait, for example increased reproduction, results in a detrimental change in another, for example decreased survival. The underlying reasoning is that resources (e.g., nutrients, energy, time) are finite and this gives rise to trade-offs in their allocation among traits, activities, or processes that compete for the same resource. Therefore, allocation of a resource to one trait means that less can be invested to other traits. This simple concept, referred to as a trade-off, has had a prominent role in our understanding of how life history variation arises.We currently know very little about how these costs of reproduction are actually incurred, since the majority of studies have focussed on the outcomes rather than the mechanisms. In the last decade, there has been substantial interest in the role of oxidative stress as a mechanism underlying the cost of reproduction and other life-history trade-offs. Oxidative stress is a complex multifaceted biochemical condition of the organism that occurs when generation of oxidative molecular damage increases (Costantini, 2008(Costantini, , 2014Metcalfe and Alonso-Alvarez, 2010;Isaksson et al., 2011). Several recent studies have, however, found weak or no support that reproductive effort increases oxidative damage (Costantini, 2014). In a recent article, Metcalfe and Monaghan (2013) have pointed out that several of these studies testing the role of oxidative stress as a cost of reproduction did not include data on non-breeding controls, making it hard to exclude seasonal or ontogenetic causes of changes in oxidative stress. They also highlighted, however, that females may tailor their own level of reproduction to avoid oxidative damage, hence it would be also important to manipulate the reproductive effort. In another article, Speakman and Garratt (2014) reinforced the idea of testing the oxidative cost of reproduction by randomly assigning animals to two groups, one of which is forced to reproduce and another one that is prevented from doing so. This is because even if individuals can choose their level of reproduction, what they cannot avoid, is an increase in metabolic rate, relative to a non-reproductive control animal. Recent experimental meta-analytic (Blount et al., 2015) work has, however, found that oxidative damage is lower in reproducing than in non-reproducing individuals, providing again little support for the oxidative cost of reproduction hypothesis.An important question then is whether non-reproducing individuals are truly appropriate controls. The answer does not seem to be so straightforward. Non-reproducing individuals may differ from reproducing individuals in several characteristics, which might make ...

High activity before breeding improves reproductive performance by enhancing mitochondrial function and biogenesis

“…The negative effects of damage from ROS have been proposed to include future ability to compete, attract mates, allocate resources to reproduction, and support processes that combat senescence (Sohal and Weindruch, 1996;von Schantz et al, 1999;Costantini, 2008;Monaghan et al, 2009;Metcalfe and Monaghan, 2013). Yet empirical evidence does not consistently show that an increase in ROS production is harmful (Speakman and Selman, 2011;Costantini, 2014Costantini, , 2016Speakman and Garratt, 2014;Blount et al, 2015;Mowry et al, 2016). In the present study, we showed no differences in ROS emission or oxidative damage in the tissues studied other than higher 4-HNE levels in liver of the females that ran and reproduced.…”

No short-term physiological costs of offspring care in a cooperatively breeding bird

“…As a result, it is not possible to identify which physiological mechanism may best mediate a cost of reproduction in this species. Nevertheless, our study compared investment in offspring care by breeders and alloparents across their natural range of variation, which has been suggested to represent a powerful comparison to explore the physiological underpinnings of the cost of reproduction (Costantini, 2016a;Speakman and Garratt, 2014). Regardless of whether manipulating investment in offspring care would have unveiled a cost of reproduction in superb starlings, our study suggests that in free-living cooperative breeders where individuals can select their contribution to parental or alloparental care, individuals did not incur a short-term cost of offspring care as measured across diverse physiological systems.…”

“…It is under these types of harsh environments (compared with a laboratory environment where food is provided ad libitum) that the cost of reproduction is most likely to be elevated and detectable (Erikstad et al, 1998;Speakman and Garratt, 2014). Second, cooperatively breeding species are ideal systems to explore how natural variation in care shapes the cost of rearing offspring (Costantini, 2016a;Speakman and Garratt, 2014) because care involves a combination of parental and alloparental forms. In superb starlings, investment in offspring care is highly variable from one individual to the next (Guindre-Parker and Rubenstein, 2018b), making it possible to explore whether individuals that invest most in caring for offspring pay a greater cost of reproduction.…”

Energetic investment associated with vitellogenesis induces an oxidative cost of reproduction

“…A relationship between reproduction and oxidative stress has been proposed by several researchers (Metcalfe & Monaghan, ), but further research is needed to define and understand the differences among species and reproductive strategies. 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, ).…”