Can environmental conditions experienced in early life influence future generations?

The consequences of early developmental conditions for performance in later life are now subjected to convergent interest from many different biological sub-disciplines. However, striking data, largely from the biomedical literature, show that environmental effects experienced even before conception can be transmissible to subsequent generations. Here, we review the growing evidence from natural systems for these cross-generational effects of early life conditions, showing that they can be generated by diverse environmental stressors, affect offspring in many ways and can be transmitted directly or indirectly by both parental lines for several generations. In doing so, we emphasize why early life might be so sensitive to the transmission of environmentally induced effects across generations. We also summarize recent theoretical advancements within the field of developmental plasticity, and discuss how parents might assemble different ‘internal’ and ‘external’ cues, even from the earliest stages of life, to instruct their investment decisions in offspring. In doing so, we provide a preliminary framework within the context of adaptive plasticity for understanding inter-generational phenomena that arise from early life conditions

Experimental demonstration that offspring fathered by old males have shorter telomeres and reduced lifespans

Offspring of older parents frequently show reduced longevity, but the mechanisms driving this so-called 'Lansing effect' are unknown. While inheritance of short telomeres from older parents could underlie this effect, studies to date in different species have found mixed results, reporting positive, negative or no association between parental age and offspring telomere length (TL). However, most of the existing evidence is from non-experimental studies in which it is difficult to exclude alternative explanations such as differential survival of parents with different telomere lengths. Here we provide evidence in the zebra finch that offspring from older parents have reduced lifespans. As a first step in disentangling possible causes, we used an experimental approach to examine whether or not we could detect pre-natal paternal effects on offspring TL. We found that zebra finch embryos fathered by old males have shorter telomeres than those produced by the same mothers but with younger fathers. Since variation in embryonic TL persists into post-natal life, and early life TL is predictive of longevity in this species, this experimental study demonstrates that a paternally driven pre-natal TL reduction could at least in part underlie the reduced lifespan of offspring from older parents

The deteriorating soma and the indispensable germline: gamete senescence and offspring fitness

The idea that there is an impenetrable barrier that separates the germline and soma has shaped much thinking in evolutionary biology and in many other disciplines. However, recent research has revealed that the so-called ‘Weismann Barrier’ is leaky, and that information is transferred from soma to germline. Moreover, the germline itself is now known to age, and to be influenced by an age-related deterioration of the soma that houses and protects it. This could reduce the likelihood of successful reproduction by old individuals, but also lead to long-term deleterious consequences for any offspring that they do produce (including a shortened lifespan). Here, we review the evidence from a diverse and multidisciplinary literature for senescence in the germline and its consequences; we also examine the underlying mechanisms responsible, emphasizing changes in mutation rate, telomere loss, and impaired mitochondrial function in gametes. We consider the effect on life-history evolution, particularly reproductive scheduling and mate choice. Throughout, we draw attention to unresolved issues, new questions to consider, and areas where more research is needed. We also highlight the need for a more comparative approach that would reveal the diversity of processes that organisms have evolved to slow or halt age-related germline deterioration

Inadequate food intake at high temperatures is related to depressed mitochondrial respiratory capacity

Animals, especially ectotherms, are highly sensitive to the temperature of their surrounding environment. Extremely high temperature, for example, induces a decline of average performance of conspecifics within a population, but individual heterogeneity in the ability to cope with elevating temperatures has rarely been studied. In this study, we examined inter-individual variation in feeding ability and consequent growth rate of juvenile brown trout Salmo trutta acclimated to a high temperature (19°C), and investigated the relationship between these metrics of whole-animal performances and among-individual variation in mitochondrial respiration capacity. Food was provided ad libitum yet intake varied ten-fold amongst individuals, resulting in some fish losing weight whilst others continued to grow. Almost half of the variation in food intake was related to variability in mitochondrial capacity: low intake (and hence growth failure) was associated with high leak respiration rates within liver and muscle mitochondria, and a lower coupling of muscle mitochondria. These observations, combined with the inability of fish with low food consumption to increase their intake despite ad libitum food levels, suggest a possible insufficient capacity of the mitochondria for maintaining ATP homeostasis. Individual variation in thermal performance is likely to confer variation in the upper limit of an organism's thermal niche and in turn affect the structure of wild populations in warming environments

Differential effects of food availability on minimum and maximum rates of metabolism

Metabolic rates reflect the energetic cost of living but exhibit remarkable variation among conspecifics, partly as a result of the constraints imposed by environmental conditions. Metabolic rates are sensitive to changes in temperature and oxygen availability, but effects of food availability, particularly on maximum metabolic rates, are not well understood. Here, we show in brown trout (Salmo trutta) that maximum metabolic rates are immutable but minimum metabolic rates increase as a positive function of food availability. As a result, aerobic scope (i.e. the capacity to elevate metabolism above baseline requirements) declines as food availability increases. These differential changes in metabolic rates likely have important consequences for how organisms partition available metabolic power to different functions under the constraints imposed by food availability

Intergenerational transfer of ageing: Parental age and offspring lifespan

The extent to which the age of parents at reproduction can affect offspring lifespan and other fitness-related traits is important in our understanding of the selective forces shaping life history evolution. In this article, the widely reported negative effects of parental age on offspring lifespan (the ‘Lansing effect’) is examined. Outlined herein are the potential routes whereby a Lansing effect can occur, whether effects might accumulate across multiple generations, and how the Lansing effect should be viewed as part of a broader framework, considering how parental age affects offspring fitness. The robustness of the evidence for a Lansing effect produced so far, potential confounding variables, and how the underlying mechanisms might best be unravelled through carefully designed experimental studies are discussed

Shorter juvenile telomere length is associated with higher survival to spawning in migratory Atlantic salmon

The risk of mortality associated with a long-distance migration will depend on an animal's physiological state, as well as the prevailing ecological conditions. Here we assess whether juvenile telomere length, which in endotherms has been shown to be a biomarker of physiological state and expected lifespan, predicts whether wild Atlantic salmon Salmo salar successfully complete their marine migration. Over 1800 juvenile fish were trapped, measured, PIT-tagged and a tissue biopsy taken when migrating as juveniles down-river towards the sea. Survivors of the marine phase of the life cycle were then re-trapped and re-sampled when returning to the river to spawn as sexually mature adults, 1.5-2.5 years later. Most individuals experienced a reduction in telomere length during the marine migratory phase of their life cycle. While the relative rate of telomere loss was greater in males than females, telomere loss was unrelated to growth at sea. Contrary to expectations, salmon that had the shortest telomeres at the time of the outward migration had the greatest probability of surviving through to the return migration. This effect, independent of body size, may indicate a trade-off between investment in readiness for marine life (which favours high glucocorticoid levels, known to increase telomere attrition in other vertebrate species) and investment in telomere maintenance. Survival was also significantly influenced by the seasonal timing of outward migration, with the fish migrating downstream earliest in the spring having the highest probability of return. This study reveals that telomere length is associated with survival, although in ways that contrast with patterns seen in endotherms. This illustrates that while telomeres may be universally important for chromosome protection, the potential for telomere dynamics to predict performance may vary across taxa

How telomere dynamics are influenced by the balance between mitochondrial efficiency, reactive oxygen species production and DNA damage

It is well known that oxidative stress is a major cause of DNA damage and telomere attrition. Most endogenous reactive oxygen species (ROS) are produced in the mitochondria, producing a link between mitochondrial function, DNA integrity and telomere dynamics. In this review we will describe how ROS production, rates of damage to telomeric DNA and DNA repair are dynamic processes. The rate of ROS production depends on mitochondrial features such as the level of inner membrane uncoupling and the proportion of time that ATP is actively being produced. However, the efficiency of ATP production (the ATP/O ratio) is positively related to the rate of ROS production, so leading to a trade-off between the body's energy requirements and its need to prevent oxidative stress. Telomeric DNA is especially vulnerable to oxidative damage due to features such as its high guanine content; while repair to damaged telomere regions is possible through a range of mechanisms, these can result in more rapid telomere shortening. There is increasing evidence that mitochondrial efficiency varies over time and with environmental context, as do rates of DNA repair. We argue that telomere dynamics can only be understood by appreciating that the optimal solution to the trade-off between energetic efficiency and telomere protection will differ between individuals and will change over time, depending on resource availability, energetic demands and life history strategy

Measurement of mitochondrial respiration in permeabilized fish gills

Physiological investigations of fish gills have traditionally been centered on the two principal functions of the gills, gas exchange and ion regulation. Mitochondrion-rich cells (MRCs) are primarily found within the gill filaments of fish, and are thought to proliferate in order to increase the ionoregulatory capacity of the gill in response to environmentally-induced osmotic challenges. However, surprisingly little attention has been paid to the metabolic function of mitochondria within fish gills. Here we describe and validate a simple protocol for the permeabilization of fish gills and subsequent measurement of mitochondrial respiration rates in vitro. Our protocol requires only small tissue samples (8 mg), it exploits the natural structure of fish gills, does not require mechanical separation of the gill tissue (so is relatively quick to perform), and yields accurate and highly reproducible measurements of respiration rates. It offers great potential for the study of mitochondrial function in gills over a wide range of fish sizes and species

Metabolic rate evolves rapidly and in parallel with the pace of life history

Metabolic rates and life history strategies are both thought to set the "pace of life", but whether they evolve in tandem is not well understood. Here, using a common garden experiment that compares replicate paired populations, we show that Trinidadian guppy (Poecilia reticulata) populations that evolved a fast-paced life history in high-predation environments have consistently higher metabolic rates than guppies that evolved a slow-paced life history in low-predation environments. Furthermore, by transplanting guppies from high- to low-predation environments, we show that metabolic rate evolves in parallel with the pace of life history, at a rapid rate, and in the same direction as found for naturally occurring populations. Together, these multiple lines of inference provide evidence for a tight evolutionary coupling between metabolism and the pace of life history