Solving the conundrum of intra-specific variation in metabolic rate: A multidisciplinary conceptual and methodological toolkit: New technical developments are opening the door to an understanding of why metabolic rate varies among individual animals of a species: New technical developments are opening the door to an understanding of why metabolic rate varies among individual animals of a species.

Researchers from diverse disciplines, including organismal and cellular physiology, sports science, human nutrition, evolution and ecology, have sought to understand the causes and consequences of the surprising variation in metabolic rate found among and within individual animals of the same species. Research in this area has been hampered by differences in approach, terminology and methodology, and the context in which measurements are made. Recent advances provide important opportunities to identify and address the key questions in the field. By bringing together researchers from different areas of biology and biomedicine, we describe and evaluate these developments and the insights they could yield, highlighting the need for more standardisation across disciplines. We conclude with a list of important questions that can now be addressed by developing a common conceptual and methodological toolkit for studies on metabolic variation in animals.

High summer temperatures are associated with poorer performance of underyearling Atlantic salmon (Salmo salar) in upland streams.

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.

Habitat restoration weakens negative environmental effects on telomere dynamics.

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.

Metabolic Rate Interacts with Resource Availability to Determine Individual Variation in Microhabitat Use in the Wild.

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.

Nutrients from salmon parents alter selection pressures on their offspring.

Organisms can modify their surrounding environment, but whether these changes are large enough to feed back and alter their evolutionary trajectories is not well understood, particularly in wild populations. Here we show that nutrient pulses from decomposing Atlantic salmon (Salmo salar) parents alter selection pressures on their offspring with important consequences for their phenotypic and genetic diversity. We found a strong survival advantage to larger eggs and faster juvenile metabolic rates in streams lacking carcasses but not in streams containing this parental nutrient input. Differences in selection intensities led to significant phenotypic divergence in these two traits among stream types. Stronger selection in streams with low parental nutrient input also decreased the number of surviving families compared to streams with high parental nutrient levels. Observed effects of parent-derived nutrients on selection pressures provide experimental evidence for key components of eco-evolutionary feedbacks in wild populations.

Links between parental life histories of wild salmon and the telomere lengths of their offspring.

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.

Telomere elongation during early development is independent of environmental temperatures in Atlantic salmon.

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 (Salmo salar) 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.

The association between parental life history and offspring phenotype in Atlantic salmon.

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 (2 versus 1 year) produced offspring that 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.

Early survival in Atlantic salmon is associated with parental genotypes at loci linked to timing of maturation.

Large effect loci often contain genes with critical developmental functions and potentially broad effects across life stages. However, their 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 behavioral 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 nutrients but not 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 of 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.

Multilocus variable-number tandem-repeat genotyping of Renibacterium salmoninarum, a bacterium causing bacterial kidney disease in salmonid fish.

BACKGROUND: Bacterial kidney disease (BKD), caused by Renibacterium salmoninarum, is a bacterial disease of fish, which is both geographically widespread and difficult to control. Previously, application of various molecular typing methods has failed to reliably discriminate between R. salmoninarum isolates originating from different host species and geographic areas. The current study aimed to utilize multilocus variable number tandem repeats (VNTR) to investigate inter-strain variation of R. salmoninarum to establish whether host-specific populations exist in Atlantic salmon and rainbow trout respectively. Such information would be valuable in risk assessment of transmission of R. salmoninarum in a multispecies aquaculture environment. RESULTS: The present analysis utilizing sixteen VNTRs distinguished 17 different haplotypes amongst 41 R. salmoninarum isolates originating from Atlantic salmon and rainbow trout in Scotland, Norway and the US. The VNTR typing system revealed two well supported groups of R. salmoninarum haplotypes. The first group included R. salmoninarum isolates originating from both Atlantic salmon and rainbow trout circulating in Scottish and Norwegian aquaculture, in addition to the type strain ATCC33209T originating from Chinook salmon in North America. The second group comprised isolates found exclusively in Atlantic salmon, of mainly wild origin, including isolates NCIB1114 and NCIB1116 associated with the original Dee disease in Scotland. CONCLUSIONS: The present study confirmed that VNTR analysis can be successfully applied to discriminate R. salmoninarum strains. There was no clear distinction between isolates originating from Atlantic salmon and rainbow trout as several haplotypes in group 1 clustered together R. salmoninarum isolates from both species. These findings indicate a potential exchange of pathogens between Atlantic salmon and rainbow trout in Scottish and Norwegian aquaculture during the last 20 years. In a scenario of expansion of rainbow trout farming into the marine environment, appropriate biosecurity measures to minimize disease occurrence are advised. The present results also suggest that R. salmoninarum isolates circulating in European aquaculture over the last 20 years are genetically distant to the wild strains originally causing BKD in the rivers Dee and Spey.

Does pre-spawning catch and release angling affect offspring telomere dynamics in Atlantic salmon?

The practice of 'catch and release' (C&R) angling confers a balance between animal welfare, conservation efforts and preserving the socio-economic interests of recreational angling. However, C&R angling can still cause exhaustion and physical injury, and often exposes the captured fish to the stress of air exposure. Therefore, the true conservation success of C&R angling depends on whether the angled individuals then survive to reproduction and whether there are any persisting effects on subsequent generations. Here we tested the hypothesis that the stress of C&R angling is then passed on to offspring. We experimentally manipulated the C&R experience of wild adult salmon prior to the spawning season. These parental fish either underwent a C&R simulation (which involved exercise with/without air exposure) or were left as control individuals. We then measured the telomere length of the arising offspring (at the larval stage of development) since previous studies have linked a shorter telomere length with reduced fitness/longevity and the rate of telomere loss is thought to be influenced by stress. Family-level telomere length was positively related to rate of growth. However, the telomere lengths of the salmon offspring were unrelated to the C&R experience of their parents. This may be due to there being no intergenerational effect of parental stress exposure on offspring telomeres, or to any potential effects being buffered by the significant telomere elongation mechanisms that are thought to occur during the embryonic and larval stages of development. While this may suggest that C&R angling has a minimal intergenerational effect on offspring fitness, there have been numerous other reports of negative C&R effects, therefore we should still be aiming to mitigate and refine such practices, in order to minimize their impacts on fish populations.

Distinct telomere differences within a reproductively bimodal common lizard population.

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. A free http://onlinelibrary.wiley.com/doi/10.1111/1365-2435.13408/suppinfo can be found within the Supporting Information of this article.