In many taxa there is considerable intraspecific variation in life-history strategies from within a single population, reflecting alternative routes through which organisms can achieve successful ...reproduction. Atlantic salmon Salmo salar (Linnaeus) show some of the greatest within-population variability in life history strategies amongst vertebrates, with multiple discrete male and female life histories co-existing and interbreeding on many spawning grounds, although the effect of the various combinations of life histories on offspring traits remains unknown. Using crosses of wild fish we show here that the life history strategy of both parents was significantly associated with a range of offspring traits. Mothers that had spent longer at sea (two versus one year) produced offspring which were heavier, longer and in better condition at the time of first feeding. However, these relationships disappeared shortly after fry had begun feeding exogenously. At this stage, the juvenile rearing environment (i.e. time spent in fresh water as juveniles) of the mother was a better predictor of offspring traits, with mothers that were faster to develop in fresh water (migrating to sea after two rather than three years of age) producing offspring that had higher maximal metabolic rates, aerobic scopes, and that grew faster. Faster developing fathers (1 year old sneaker males) tended to produce offspring that had higher maximal metabolic rates, were in better body condition and grew faster. The results suggest that both genetic effects and those related to parental early and late life history contribute to offspring traits.
Large effects loci often contain genes with critical developmental functions with potentially broad effects across life-stages. However, the life-stage-specific fitness consequences are rarely ...explored. In Atlantic salmon, variation in two large-effect loci, six6 and vgll3, is linked to age at maturity, and several physiological and behavioural traits in early life. By genotyping the progeny of wild Atlantic salmon that were planted into natural streams with nutrient manipulations, we tested if genetic variation in these loci is associated with survival in early life. We found that higher early life survival was linked to the genotype associated with late maturation in the vgll3, but with early maturation in the six6 locus. These effects were significant in high-nutrient, but not in in low-nutrient streams. The differences in early survival were not explained by additive genetic effects in the offspring generation, but by maternal genotypes in the six6 locus, and by both parents' genotypes in the vgll3 locus. Our results suggest that indirect genetic effects by large-effect loci can be significant determinants of offspring fitness. This study demonstrates an intriguing case of how large-effect loci can exhibit complex fitness associations across life stages in the wild and indicates that predicting evolutionary dynamics is difficult.
Habitat quality can have far‐reaching effects on organismal fitness, an issue of concern given the current scale of habitat degradation. Many temperate upland streams have reduced nutrient levels due ...to human activity. Nutrient restoration confers benefits in terms of invertebrate food availability and subsequent fish growth rates. Here we test whether these mitigation measures also affect the rate of cellular ageing of the fish, measured in terms of the telomeres that cap the ends of eukaryotic chromosomes. We equally distributed Atlantic salmon eggs from the same 30 focal families into 10 human‐impacted oligotrophic streams in northern Scotland. Nutrient levels in five of the streams were restored by simulating the deposition of a small number of adult Atlantic salmon Salmo salar carcasses at the end of the spawning period, while five reference streams were left as controls. Telomere lengths and expression of the telomerase reverse transcriptase (TERT) gene that may act to lengthen telomeres were then measured in the young fish when 15 months old. While TERT expression was unrelated to any of the measured variables, telomere lengths were shorter in salmon living at higher densities and in areas with a lower availability of the preferred substrate (cobbles and boulders). However, the adverse effects of these habitat features were much reduced in the streams receiving nutrients. These results suggest that adverse environmental pressures are weakened when nutrients are restored, presumably because the resulting increase in food supply reduces levels of both competition and stress.
Different strategies of reproductive mode, either oviparity (egg‐laying) or viviparity (live‐bearing), will be associated with a range of other life‐history differences that are expected to affect ...patterns of ageing and longevity. It is usually difficult to compare the effects of alternative reproductive modes because of evolutionary and ecological divergence. However, the very rare exemplars of reproductive bimodality, in which different modes exist within a single species, offer an opportunity for robust and controlled comparisons.
One trait of interest that could be associated with life history, ageing and longevity is the length of the telomeres, which form protective caps at the chromosome ends and are generally considered a good indicator of cellular health. The shortening of these telomeres has been linked to stressful conditions; therefore, it is possible that differing reproductive costs will influence patterns of telomere loss. This is important because a number of studies have linked a shorter telomere length to reduced survival.
Here, we have studied maternal and offspring telomere dynamics in the common lizard (Zootoca vivipara). Our study has focused on a population where oviparous and viviparous individuals co‐occur in the same habitat and occasionally interbreed to form admixed individuals.
While viviparity confers many advantages for offspring, it might also incur substantial costs for the mother, for example require more energy. Therefore, we predicted that viviparous mothers would have relatively shorter telomeres than oviparous mothers, with admixed mothers having intermediate telomere lengths. There is thought to be a heritable component to telomere length; therefore, we also hypothesized that offspring would follow the same pattern as the mothers.
Contrary to our predictions, the viviparous mothers and offspring had the longest telomeres, and the oviparous mothers and offspring had the shortest telomeres. The differing telomere lengths may have evolved as an effect of the life‐history divergence between the reproductive modes, for example due to the increased growth rate that viviparous individuals may undergo to reach a similar size at reproduction.
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In partially migratory species, individuals either migrate at some point(s) in life or reside within their natal habitat throughout life. For salmonid fish, migration creates opportunities for ...feeding and growth, but it is also associated with increased mortality risk. Such trade‐offs likely differ between the sexes, since reproductive output is more closely tied to body size in females than males. However, testing hypotheses on sex‐specific migratory behaviour in would‐be first‐time migratory salmonids is difficult, since sexes are generally morphologically indistinguishable prior to maturation. Previous studies have evaluated the influence of sex on migration based on dissection of migratory juveniles or the sex ratio of returning adults. However, both approaches are potentially biased by differential survival during migration. Here, we utilise advances in minimally invasive genetic sex‐determination methods for salmonids to investigate sex‐specific, spring out‐migration propensity in potamodromous brown trout (Salmo trutta) in a pre‐Alpine, central European lake. We show that there are marked differences in migratory behaviour between males and females, with small (~10 cm) females being approximately twice as likely to migrate out of their natal river in spring compared to similarly sized males, which generally migrate for the first time at larger sizes (in similar proportions to larger females). This study highlights how novel genetic sex‐determination techniques can provide insight into the sex‐ and size‐specific life‐history trade‐offs that shape migration propensity. Moving forward, these techniques should become useful tools for ecologists and fisheries managers.
Ecological pressures such as competition can lead individuals within a population to partition resources or habitats, but the underlying intrinsic mechanisms that determine an individual’s resource ...use are not well understood. Here we show that an individual’s own energy demand and associated competitive ability influence its resource use, but only when food is more limiting. We tested whether intraspecific variation in metabolic rate leads to microhabitat partitioning among juvenile Atlantic salmon (Salmo salar) in natural streams subjected to manipulated nutrient levels and subsequent per capita food availability. We found that individual salmon from families with a higher baseline (standard) metabolic rate (which is associated with greater competitive ability) tended to occupy faster-flowing water, but only in streams with lower per capita food availability. Faster-flowing microhabitats yield more food, but high metabolic rate fish only benefited from faster growth in streams with high food levels, presumably because in low-food environments the cost of a high metabolism offsets the benefits of acquiring a productive microhabitat. The benefits of a given metabolic rate were thus context dependent. These results demonstrate that intraspecific variation in metabolic rate can interact with resource availability to determine the spatial structuring of wild populations.
The importance of parental contributions to offspring development and subsequent performance is self‐evident at a genomic level; however, parents can also affect offspring fitness by indirect genetic ...and environmental routes. The life history strategy that an individual adopts will be influenced by both genes and environment; and this may have important consequences for offspring. Recent research has linked telomere dynamics (i.e., telomere length and loss) in early life to future viability and longevity. Moreover, a number of studies have reported a heritable component to telomere length across a range of vertebrates, although the effects of other parental contribution pathways have been far less studied. Using wild Atlantic salmon with different parental life histories in an experimental split‐brood in vitro fertilization mating design and rearing the resulting families under standardized conditions, we show that there can be significant links between parental life history and offspring telomere length (studied at the embryo and fry stage). Maternal life history traits, in particular egg size, were most strongly related to offspring telomere length at the embryonic stage, but then became weaker through development. In contrast, paternal life history traits, such as the father's growth rate in early life, had a greater association in the later stages of offspring development. However, offspring telomere length was not significantly related to either maternal or paternal age at reproduction, nor to paternal sperm telomere length. This study demonstrates both the complexity and the importance of parental factors that can influence telomere length in early life.
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 life span, predicts whether wild Atlantic salmon Salmo salar successfully complete their marine migration.
Over 1,800 juvenile fish were trapped, measured, passive integrated transponder 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.
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There is increasing evidence from endothermic vertebrates that telomeres, which cap the ends of chromosomes and play an important role in chromosome protection, decline in length during postnatal ...life and are a useful indicator of physiological state and expected lifespan. However, much less is currently known about telomere dynamics in ectothermic vertebrates, which are likely to differ from that of endotherms, at least in part due to the sensitivity of ectotherm physiology to environmental temperature. We report here on an experiment in which Atlantic salmon (
) were reared through the embryonic and larval stages of development, and under differing temperatures, in order to examine the effects of environmental temperature during early life on telomere dynamics, oxidative DNA damage and cellular proliferation. Telomere length significantly increased between the embryonic and larval stages of development. Contrary to our expectations, variation in telomere length at the end of the larval stage was unrelated to either cell proliferation rate or the relative level of oxidative DNA damage, and did not vary between the temperature treatments. This study suggests that salmon are able to restore the length of their telomeres during early development, which may possibly help to buffer potentially harmful environmental effects experienced in early life.
Future warming scenarios are predicted to result in an increased frequency of high, and potentially stressful, temperatures in aquatic ecosystems. Here we examined whether the performance of wild ...underyearling Atlantic salmon (Salmo salar) in Scottish streams stocked with identical egg densities was influenced by thermal stress. Biomass and density declined with degree hours exceeding 23°C, indicating apparent mortality or emigration as a possible result of exposure to high temperatures. These results strengthen the need for further action such as riparian tree planting to reduce stream summer temperatures.
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