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

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.

How important is hidden phenotypic plasticity arising from alternative but converging developmental trajectories, and what limits it?

Developmental plasticity -- the capacity for a genotype to develop into different phenotypes, depending on the environment - is typically viewed from the perspective of the resulting phenotype. Thus, if development is viewed as a trajectory towards a target, then developmental plasticity allows environmentally induced alterations to the target. However, there can also be variations in the trajectory. This is seen with compensatory responses, for instance where growth accelerates after an earlier period of food shortage, or where investment in sexual ornaments is maintained even when resources are limiting. If the compensation is complete, the adult phenotype can appear 'normal' (i.e. the different developmental trajectories converge on the same target). However, alternative trajectories to a common target can have multiple long-term consequences, including altered physiological programming and rates of senescence, possibly owing to trade-offs between allocating resources to the prioritized trait versus to body maintenance. This suggests that plasticity in developmental trajectories towards a common target leads to variation in the resilience and robustness of the adult body. This form of developmental plasticity is far more hidden than plasticity in final adult target, but it may be more common. Here, I discuss the causes, consequences and limitations of these different kinds of plasticity, with a special focus on whether they are likely to be adaptive. I emphasize the need to study plasticity in developmental trajectories, and conclude with suggestions for future research to tease apart the different forms of developmental plasticity and the factors that influence their evolution and expression.

Intergenerational plasticity aligns with temperature-dependent selection on offspring metabolic rates.

Metabolic rates are linked to key life-history traits that are thought to set the pace of life and affect fitness, yet the role that parents may have in shaping the metabolism of their offspring to enhance survival remains unclear. Here, we investigated the effect of temperature (24°C or 30°C) and feeding frequency experienced by parent zebrafish (Danio rerio) on offspring phenotypes and early survival at different developmental temperatures (24°C or 30°C). We found that embryo size was larger, but survival lower, in offspring from the parental low food treatment. Parents exposed to the warmer temperature and lower food treatment also produced offspring with lower standard metabolic rates-aligning with selection on embryo metabolic rates. Lower metabolic rates were correlated with reduced developmental and growth rates, suggesting selection for a slow pace of life. Our results show that intergenerational phenotypic plasticity on offspring size and metabolic rate can be adaptive when parent and offspring temperatures are matched: the direction of selection on embryo size and metabolism aligned with intergenerational plasticity towards lower metabolism at higher temperatures, particularly in offspring from low-condition parents. These findings provide evidence for adaptive parental effects, but only when parental and offspring environments match. This article is part of the theme issue 'The evolutionary significance of variation in metabolic rates'.

Unpredictability of maternal environment shapes offspring behaviour without affecting stress-induced cortisol in an annual vertebrate.

Exposure of females to stressful conditions during pregnancy or oogenesis has a profound effect on the phenotype of their offspring. For example, offspring behavioural phenotype may show altered patterns in terms of the consistency of behavioural patterns and their average level of performance. Maternal stress can also affect the development of the stress axis in offspring leading to alterations in their physiological stress response. However, the majority of evidence comes from studies utilising acute stressors or exogenous glucocorticoids, and little is known about the effect of chronic maternal stress, particularly in the context of stress lasting throughout entire reproductive lifespan. To bridge this knowledge gap, we exposed female sticklebacks to stressful and unpredictable environmental conditions throughout the breeding season. We quantified the activity, sheltering and anxiety-like behaviour of offspring from three successive clutches of these females, and calculated Intra-class Correlation Coefficients for these behaviours in siblings and half-siblings. We also exposed offspring to an acute stressor and measured their peak cortisol levels. An unpredictable maternal environment had no modifying effect on inter-clutch acute stress responsivity, but resulted in diversification of offspring behaviour, indicated by an increased between-individual variability within families. This may represent a bet-hedging strategy, whereby females produce offspring differing in behavioural phenotype, to increase the chance that some of these offspring will be better at coping with the anticipated conditions.

Surrogacy and the law in the UK.

Surrogacy is a method of assisted reproduction in which a woman bears a child on behalf of a couple or individual with the intention of handing over care of the child to the intending parent(s) at or soon after birth. The law surrounding surrogacy is complex for healthcare professionals, surrogates and intending parent(s) to navigate. This review article summarises the laws and potential legal complications of surrogacy in the UK. While altruistic surrogacy is permitted, commercial surrogacy is outlawed in this country. Both traditional and gestational surrogacy may be performed and UK law now also permits surrogacy for same sex couples, unmarried couples and single individuals as intending parent(s). Legal parenthood of the child is transferred from the surrogate to the intending parent(s) via application for a parental order between 6 weeks and 6 months after birth. Legal complications include time restrictions for parental order applications and breaches of reasonable payments to surrogates.

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.

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.

Ageing across the great divide: tissue transformation, organismal growth and temperature shape telomere dynamics through the metamorphic transition.

Telomere attrition is considered a useful indicator of cellular and whole-organism ageing rate. While approximately 80% of animal species undergo metamorphosis that includes extensive tissue transformations (involving cell division, apoptosis, de-differentiation and de novo formation of stem cells), the effect on telomere dynamics is unknown. We measured telomeres in Xenopus laevis developing from larvae to adults under contrasting environmental temperatures. Telomere dynamics were linked to the degree of tissue transformation during development. Average telomere length in gut tissue increased dramatically during metamorphosis, when the gut shortens by 75% and epithelial cells de-differentiate into stem cells. In the liver (retained from larva) and hindlimb muscle (newly formed before metamorphosis), telomeres gradually shortened until adulthood, likely due to extensive cell division. Tail muscle telomere lengths were constant until tail resorption, and those in heart (retained from larva) showed no change over time. Telomere lengths negatively correlated with larval growth, but for a given growth rate, telomeres were shorter in cooler conditions, suggesting that growing in the cold is more costly. Telomere lengths were not related to post-metamorphic growth rate. Further research is now needed to understand whether telomere dynamics are a good indicator of ageing rate in species undergoing metamorphosis.

Geothermal stickleback populations prefer cool water despite multigenerational exposure to a warm environment.

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°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, we suggest that preferred temperature alone may be a poor indicator of a population's adaptive potential to a novel thermal environment.

Testing the predictability of morphological evolution in contrasting thermal environments.

Gaining the ability to predict population responses to climate change is a pressing concern. Using a "natural experiment," we show that testing for divergent evolution in wild populations from contrasting thermal environments provides a powerful approach, and likely an enhanced predictive power for responses to climate change. 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 focused on morphological traits across six pairs from warm and cold habitats. We found that fish from warm habitats tended to have a deeper mid-body, a subterminally orientated jaw, steeper craniofacial profile, and deeper caudal region relative to fish from cold habitats. Our common garden experiment showed that most of these differences were heritable. Population age did not appear to influence the magnitude or type of thermal divergence, but similar types of divergence between thermal habitats were more prevalent across allopatric than sympatric population pairs. These findings suggest that morphological divergence in response to thermal habitat, despite being relatively complex and multivariate, are predictable to a degree. Our data also suggest that the potential for migration of individuals between different thermal habitats may enhance nonparallel evolution and reduce our ability to predict responses to climate change.

A warmer environment can reduce sociability in an ectotherm.

The costs and benefits of being social vary with environmental conditions, so individuals must weigh the balance between these trade-offs in response to changes in the environment. Temperature is a salient environmental factor that may play a key role in altering the costs and benefits of sociality through its effects on food availability, predator abundance, and other ecological parameters. In ectotherms, changes in temperature also have direct effects on physiological traits linked to social behaviour, such as metabolic rate and locomotor performance. In light of climate change, it is therefore important to understand the potential effects of temperature on sociality. Here, we took the advantage of a 'natural experiment' of threespine sticklebacks from contrasting thermal environments in Iceland: geothermally warmed water bodies (warm habitats) and adjacent ambient-temperature water bodies (cold habitats) that were either linked (sympatric) or physically distinct (allopatric). We first measured the sociability of wild-caught adult fish from warm and cold habitats after acclimation to a low and a high temperature. At both acclimation temperatures, fish from the allopatric warm habitat were less social than those from the allopatric cold habitat, whereas fish from sympatric warm and cold habitats showed no differences in sociability. To determine whether differences in sociability between thermal habitats in the allopatric population were heritable, we used a common garden breeding design where individuals from the warm and the cold habitat were reared at a low or high temperature for two generations. We found that sociability was indeed heritable but also influenced by rearing temperature, suggesting that thermal conditions during early life can play an important role in influencing social behaviour in adulthood. By providing the first evidence for a causal effect of rearing temperature on social behaviour, our study provides novel insights into how a warming world may influence sociality in animal populations.

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.

Timing of reproduction modifies transgenerational effects of chronic exposure to stressors in an annual vertebrate.

Stressful environmental conditions can shape both an individual's phenotype and that of its offspring. However, little is known about transgenerational effects of chronic (as opposed to acute) stressors, nor whether these vary across the breeding lifespan of the parent. We exposed adult female (F0 generation) three-spined sticklebacks (Gasterosteus aculeatus) to chronic environmental stressors and compared their reproductive allocation with that of non-exposed controls across early, middle and late clutches produced within the single breeding season of this annual population. There was a seasonal trend (but no treatment difference) in F0 reproductive allocation, with increases in egg mass and fry size in late clutches. We then tested for transgenerational effects in the non-exposed F1 and F2 generations. Exposure of F0 females to stressors resulted in phenotypic change in their offspring and grandoffspring that were produced late in their breeding lifespan: F1 offspring produced from the late-season clutches of stressor-exposed F0 females had higher early life survival, and subsequently produced heavier eggs and F2 fry that were larger at hatching. Changed maternal allocation due to a combination of seasonal factors and environmental stressors can thus have a transgenerational effect by influencing the reproductive allocation of daughters, especially those born late in life.

Nutrient limitation in Atlantic salmon rivers and streams: Causes, consequences, and management strategies.

Freshwater catchments can experience nutrient deficits that result in reduced primary and secondary productivity. The most commonly limiting nutrients are nitrogen and phosphorus, either separately or together. This review considers the impact of increasing nutrient limitation in temperate basin stream and river systems, focusing on upland areas that currently or previously supported wild Atlantic salmon (Salmo salar) populations.Anthropogenic changes to land use and increases in river barriers have altered upland nutrient dynamics, with particular impacts on salmon and other migratory fish species which may be net importers of nutrients to upland streams. Declining salmon populations may further reduce nutrient sources, reducing ecosystem and fisheries productivity below desired levels.Experimental manipulations of nutrient levels have examined the impacts of this cultural oligotrophication. There is evidence that growth and biomass of juvenile salmon can be increased via appropriate additions of nutrients, offering potential as a conservation tool. However, further research is required to understand the long-term effects of these additions on salmon populations and stream ecosystems, and to assess the vulnerability of downstream habitats to eutrophication as a result.Although purposeful nutrient addition with the aim of enhancing and conserving salmonid populations may be justified in some cases, it should be undertaken in an adaptive management framework. In addition, nutrient addition should be linked to nutrient retention and processing, and integrated into large-scale habitat restoration and recovery efforts.Both the scientific and the management community should recognize that the ecological costs and benefits associated with adding nutrients to salmon streams may change in a non-stationary world.

The Evolution of Offspring Size: a Metabolic Scaling Perspective.

Size at the start of life reflects the initial per offspring parental investment - including both the embryo and the nutrients supplied to it. Initial offspring size can vary substantially both within and among species. Within species, increasing offspring size can enhance growth, reproduction, competitive ability, and reduce susceptibility to predation and starvation later in life, that can ultimately increase fitness. Previous work has suggested that the fitness benefits of larger offspring size may be driven by energy expenditure during development - or how offspring metabolic rate scales with offspring size. Despite the importance of early life energy expenditure in shaping later life fitness trajectories, consideration of among-species scaling of metabolic rate at the time of birth as a potential source of general metabolic scaling patterns has been overlooked by theory. Here we review the patterns and processes of energy expenditure at the start of life when mortality is often greatest. We compile existing data on metabolic rate and offspring size for 191 ectotherm species spanning eight phyla and use phylogenetically-controlled methods to quantify among-species scaling patterns. Across a 109-fold mass range, we find that offspring metabolic rate scales hypometrically with size, with an overall scaling exponent of 0.66. This exponent varies across ontogenetic stage and feeding activity, but is consistently hypometric, including across environmental temperatures. Despite differences in parental investment, life history and habitat, large-offspring species use relatively less energy as a proportion of size, compared with small-offspring species. Greater residual energy can be used to fuel the next stages of life, particularly in low resource environments. Based on available evidence, we conclude that, while large knowledge gaps remain, the evolution of offspring size is likely shaped by context-dependent selection acting on correlated traits, including metabolic rates maintaining hypometric scaling, that operates within broader physical constraints.

Inter-individual variation in mitochondrial phosphorylation efficiency predicts growth rates in ectotherms at high temperatures.

There is increasing evidence that aquatic ectotherms are especially vulnerable to global warming since their metabolic demands increase with ambient temperature while water-oxygen content decreases. The possible role of shrinking aerobic scope in limiting performance has been much discussed; however, less attention has been given to whether tissue-level changes in the efficiency of oxygen usage occur at elevated temperatures. Here, we show that this varies widely among individuals, with consequences for performance. We examined the inter-individual variation in growth rate and mitochondrial function from white muscle and liver of brown trout (Salmo trutta) acclimated to either high (19.5°C) or near-optimal temperature (12°C). Liver (but not muscle) mitochondria showed a positive relationship between growth rate and maximal oxidative phosphorylation at both temperatures, and a negative relationship between growth rate and ROS release. There was a positive correlation in both tissues between individual mitochondrial phosphorylation efficiency and growth rate, but only at 19.5°C. In this representative of aquatic ectotherms, an individual's liver mitochondrial efficiency thus seems to dictate its capacity to grow at elevated temperatures. This suggests that individual heterogeneity in cellular function may cause variation in the thermal limits of aquatic ectotherms and could adversely affect wild populations in warming environments.

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 could 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) and 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 parts 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 (less than 20%) of the consistent among-individual differences we observed. Our results demonstrate that prenatal conditions can programme consistent and long-lasting differences in mitochondrial function, which could potentially underlie among-individual variation in performance and health state.

Does the match between individual and group behavior matter in shoaling sticklebacks?

In animals living in groups, the social environment is fundamental to shaping the behaviors and life histories of an individual. A mismatch between individual and group behavior patterns may have disadvantages if the individual is incapable of flexibly changing its state in response to the social environment that influences its energy gain and expenditure. We used different social groups of juvenile three-spined sticklebacks (Gasterosteus aculeatus) with experimentally manipulated compositions of individual sociability to study the feedback between individual and group behaviors and to test how the social environment shapes behavior, metabolic rate, and growth. Experimentally created unsociable groups, containing a high proportion of less sociable fish, showed bolder collective behaviors during feeding than did corresponding sociable groups. Fish within groups where the majority of members had a level of sociability similar to their own gained more mass than did those within mismatched groups. Less sociable individuals within sociable groups tended to have a relatively low mass but a high standard metabolic rate. A mismatch between the sociability of an individual and that of the majority of the group in which it is living confers a growth disadvantage probably due to the expression of nonadaptive behaviors that increase energetic costs.

Surrogacy and the law in the UK.

Surrogacy is a method of assisted reproduction in which a woman bears a child on behalf of a couple or individual with the intention of handing over care of the child to the intending parent(s) at or soon after birth. The law surrounding surrogacy is complex for healthcare professionals, surrogates and intending parent(s) to navigate. This review article summarises the laws and potential legal complications of surrogacy in the UK. While altruistic surrogacy is permitted, commercial surrogacy is outlawed in this country. Both traditional and gestational surrogacy may be performed and UK law now also permits surrogacy for same sex couples, unmarried couples and single individuals as intending parent(s). Legal parenthood of the child is transferred from the surrogate to the intending parent(s) via application for a parental order between 6 weeks and 6 months after birth. Legal complications include time restrictions for parental order applications and breaches of reasonable payments to surrogates.