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Metcalfe, N. B.

Publications and source records attributed to Metcalfe, N. B..

8 recordsLinked to original sources

Seasonal decline in mitochondrial plasticity in the three-spined stickleback

Mitochondrial plasticity enables ectothermic animals to maintain performance under changing thermal conditions, but whether this ability declines through adulthood is unknown. We explored changes in mitochondrial plasticity in the three-spined stickleback (Gasterosteus aculeatus), a temperate fish that in many populations has a single breeding season over which it produces multiple clutches and then dies. Wild-caught fish were exposed to one of three thermal regimes: remaining at 12 {degrees}C, switching to constant warm (21 {degrees}C) or diel cycling (12-21 {degrees}C) for three weeks at either the beginning or end of the season. We quantified both phosphorylating and non-ATP-producing (OXPHOS and LEAK) respiration in isolated muscle mitochondria, and oxidative control efficiency (OxCE). Early in the breeding season, young fish responded to elevated temperatures by adjusting both their capacity for ATP production and non-ATP-production respiration, but this mitochondrial plasticity declined over the season. OxCE was unaffected by time of season or temperature treatment. Changing body condition was unrelated to mitochondrial function. Our findings indicate that mitochondrial plasticity declines across adult life, potentially limiting thermal resilience in older individuals, the first time this has been reported in an ectotherm. This highlights the need to account for age-related physiological changes in capacity when predicting species responses to environmental change.

evolutionary biology↗

Genetic diversity, population structure and differentiation of farmed and wild African catfish (Clarias gariepinus) in Nigeria

The African catfish (Clarias gariepinus) is a commercially important species, for both fisheries and aquaculture, and is now the most commonly farmed fish in sub-Saharan Africa. However, knowledge about the genetic diversity and population structure of wild and farmed populations, which is crucial for effective conservation and sustainable aquaculture management, is scarce. Using mitochondrial DNA (mtDNA) cytochrome c oxidase 1 gene (COI) sequencing and genomic analysis using triple restriction site-associated DNA sequencing (3RAD), we investigated the genetic diversity and population structure of farmed and wild C. gariepinus populations from Nigeria, including an albino form found in the wild. Eleven COI haplotypes were identified, of which seven were unique to wild samples. Wild sampling sites had a slightly broader range and higher maximum values for observed heterozygosity (Ho = 0.109 - 0.165), expected heterozygosity (He = 0.111 - 0.216), and nucleotide diversity (pi = 0.125 - 0.225) compared to the farmed populations (Ho = 0.118 - 0.147, He = 0.112-0.144, pi = 0.117 - 0.151). Conversely, genetic differentiation (Fst) was higher among farmed sampling sites compared to the wild ones and there was high genetic differentiation between the farmed and wild C. gariepinus sampling sites (Fst = 0.31 - 0.47). Despite evidence for admixture for both farmed and wild fish, there was little evidence of admixture between the two groups. Nevertheless, both mtDNA and 3RAD data strongly suggested that the albino fish, collected from the wild, were in fact farm escapees. Despite overall differentiation farmed genotypes suggesting that overall genetic integrity of wild fish has been maintained, this evidence of escape provides a warning about potential risks of increasing aquaculture activities. Specifically, this indicates the need for greater regulation of fish farms to monitor and reduce the risk of escapes.

genomics↗

Early survival in Atlantic salmon is associated with parental genotype at loci linked to timing of maturation late in life

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.

evolutionary biology↗

Experimental demonstration of prenatal programming of mitochondrial aerobic metabolism lasting until adulthood

It is increasingly being postulated that among-individual variation in mitochondrial function underlies variation in individual performance (e.g. growth rate) and state of health. It has been suggested (but not adequately tested) that environmental conditions experienced before birth have been suggested to programme postnatal mitochondrial function, with persistent effects potentially lasting into adulthood. We tested this hypothesis in an avian model by experimentally manipulating prenatal conditions (incubation temperature and stability), then measuring mitochondrial aerobic metabolism in blood cells from the same individuals during the middle of the growth period and at adulthood. Mitochondrial aerobic metabolism changed markedly across life stages, and part of these age-related changes were influenced by the prenatal temperature conditions. A high incubation temperature induced a consistent and long-lasting increase in mitochondrial aerobic metabolism. Postnatal mitochondrial aerobic metabolism was positively associated with oxidative damage on DNA but not telomere length. While we detected significant within-individual consistency in mitochondrial aerobic metabolism across life-stages, the prenatal temperature regime only accounted for a relatively small proportion (<20%) of the consistent among-individual differences we observed. Our results demonstrate that prenatal conditions can program consistent and long-lasting differences in mitochondrial function, which could potentially underlie among-individual variation in performance and health state.

physiology↗

Ageing before birth: pace and stability of prenatal growth affect telomere dynamics

Pre-natal effects on telomere length are increasingly recognized as a potential contributor to the developmental origin of health and adult diseases. While it is becoming clear that telomere length is strongly influenced by pre-natal conditions, the factors affecting telomere dynamics during embryogenesis remain poorly understood. We manipulated both the pace and stability of prenatal growth using incubation temperature in Japanese quail and investigated the impact on telomere dynamics from embryogenesis to adulthood, along with potential drivers of telomere shortening such as oxidative damage and prenatal glucocorticoid levels. Telomere length was not affected by these manipulations for the first 75% of prenatal development, but was reduced at hatching in response to both experimentally induced fast embryo growth and growth instability. These early-life effects on telomere length persisted until adulthood. The effect of developmental instability on telomere length at hatching was potentially mediated by an increased secretion of glucocorticoid hormones during development. Both the pace and the stability of prenatal growth appear as key factors determining telomere length and dynamics up to adulthood, with fast and unstable embryo growth leading to short telomeres with the potential for adverse associated outcomes in terms of reduced longevity and greater risk of disease.

physiology↗

Reduction in standard metabolic rate after multigenerational exposure to elevated temperatures in the wild

O_LIIn light of global climate change, there is a pressing need to understand and predict the capacity of populations to respond to rising temperatures. Metabolic rate is a key trait that is likely to influence the ability to cope with climate change. Yet, empirical and theoretical work on metabolic rate responses to temperature changes has so far produced mixed results and conflicting predictions. C_LIO_LIOur study addresses this issue using a novel approach of comparing fish populations in geothermally warmed lakes and adjacent ambient-temperature lakes in Iceland. This unique natural experiment provides repeated and independent examples of populations experiencing contrasting thermal environments for many generations over a small geographic scale, thereby avoiding the confounding factors associated with latitudinal or elevational comparisons. Using Icelandic sticklebacks from three warm and three cold habitats, we measured individual metabolic rates across a range of acclimation temperatures to obtain reaction norms for each population. C_LIO_LIWe found a general pattern for a lower standard metabolic rate in sticklebacks from warm habitats when measured at a common temperature, as predicted by Kroghs rule. Metabolic rate differences between warm- and cold-habitat sticklebacks were more pronounced at more extreme acclimation temperatures, suggesting the release of cryptic genetic variation upon exposure to novel conditions, which can reveal hidden evolutionary potential. We also found a stronger divergence in metabolic rate between thermal habitats in allopatry than sympatry, indicating that gene flow may constrain physiological adaptation when dispersal between warm and cold habitats is possible. C_LIO_LIIn sum, our study suggests that fish may diverge toward a lower standard metabolic rate in a warming world, but this might depend on connectivity and gene flow between different thermal habitats. C_LI

physiology↗

Temperature preference does not evolve in sticklebacks despite multigenerational exposure to elevated temperatures

Given the threat of climate change to biodiversity, a growing number of studies are investigating the potential for organisms to adapt to rising temperatures. Earlier work has predicted that physiological adaptation to climate change will be accompanied by a shift in temperature preferences, but empirical evidence for this is lacking. Here, we test whether exposure to different thermal environments has led to changes in preferred temperatures in the wild. Our study takes advantage of a natural experiment in Iceland, where freshwater populations of threespine sticklebacks (Gasterosteus aculeatus) are found in waters warmed by geothermal activity year-round (warm habitats), adjacent to populations in ambient-temperature lakes (cold habitats). We used a shuttle-box approach to measure temperature preferences of wild-caught sticklebacks from three warm-cold population pairs. Our prediction was that fish from warm habitats would prefer higher water temperatures than those from cold habitats. We found no support for this, as fish from both warm and cold habitats had an average preferred temperature of 13{degrees}C. Thus, our results challenge the assumption that there will be a shift in ectotherm temperature preferences in response to climate change. In addition, since warm-habitat fish can persist at relatively high temperatures despite a lower temperature preference, this suggests that preferred temperature alone may be a poor indicator of a populations adaptive potential to a novel thermal environment.

evolutionary biology↗

Testing the predictability of morphological evolution in naturally warmed stickleback populations

In light of climate change, the ability to predict evolutionary responses to temperature changes is of central importance for conservation efforts. Prior work has focused on exposing model organisms to different temperatures for just one or a few generations under laboratory conditions. Using a natural experiment, we show that studying parallel evolution in wild populations from contrasting thermal environments presents a more powerful approach for understanding and predicting responses to climate change. More specifically, we used a unique study system in Iceland, where freshwater populations of threespine sticklebacks (Gasterosteus aculeatus) are found in waters warmed by geothermal activity, adjacent to populations in ambient-temperature water. We used three sympatric and three allopatric warm-cold population pairs to test for repeated patterns of morphological divergence in relation to thermal habitat. We found that thermal habitat explained over 50% of body shape variation: fish from warm habitats had a deeper mid-body, a shorter jaw, and smaller eyes. Our common garden experiment showed that most of these morphological differences between thermal habitats were heritable. Lastly, absence of gene flow seems to facilitate parallel divergence across thermal habitats: all three allopatric population pairs were on a common evolutionary trajectory, whereas sympatric pairs followed different trajectories. Our findings therefore suggest that morphological responses to rising temperatures can be predictable when there is limited gene flow. On the other hand, migration of individuals between different thermal habitats or microhabitats can exaggerate nonparallel evolution and reduce our ability to predict evolutionary responses.

evolutionary biology↗