Early Life Survival Research Articles

Season-specific genetic variation underlies early-life migration in a partially migratory bird.

Eco-evolutionary responses to environmentally induced selection fundamentally depend on magnitudes of genetic variation underlying traits that facilitate population persistence. Additive genetic variances and associated heritabilities can vary across environmental conditions, especially for labile phenotypic traits expressed through early life. However, short-term seasonal dynamics of genetic variances are rarely quantified in wild populations, precluding inference on eco-evolutionary outcomes in seasonally dynamic systems. This limitation applies to seasonal migration versus residence, constituting one key trait where rapid microevolution could rescue partially migratory populations from changing seasonal environments. We fitted novel quantitative genetic 'capture-recapture animal models' to multi-generational pedigree and year-round resighting data from 11 cohorts of European shags (Gulosus aristotelis), to estimate season-specific additive genetic variances in liabilities to migrate, and in resulting expression of migration, in juveniles' first autumn and winter. We demonstrate non-negligible genetic variation underlying early-life migration, with twice as large additive genetic variances and heritabilities in autumn than winter. Since early-life survival selection on migration typically occurs in winter, highest genetic variation and strongest selection are seasonally desynchronized. Our results reveal complex within- and among-year dynamics of early-life genetic and phenotypic variation, demonstrating that adequate inference of eco-evolutionary outcomes requires quantifying microevolutionary potential on appropriate scales and seasonal timeframes.

Digest: Large-effect loci involved in maturation timing affect the early survival of Atlantic salmon.

How might variation in genomic regions that impact many traits modulate fitness across different life stages? Aykanat et al. (2024) show that two large-effect loci associated with age at maturity, six6 and vgll3, impact the survival of wild Atlantic salmon (Salmo salar) through nutrient-dependent, indirect genetic effects. Specifically, the late maturation allele in parental vgll3, and the early maturation allele in maternal six6, increase survival in early life under high nutrient conditions.

A fine-scale examination of parturition timing in temperate ungulates.

Parturition timing has long been a topic of interest in ungulate research. However, few studies have examined parturition timing at fine scale (e.g., <1 day). Predator activity and environmental conditions can vary considerably with diel timing, which may result in selective pressure for parturition to occur during diel times that maximize the likelihood of neonate survival. We monitored parturition events and early-life survival of elk (Cervus canadensis) and mule deer (Odocoileus hemionus) in Utah, USA to better understand diel timing of parturition in temperate ungulates. Diel timing of parturition was moderately synchronous among conspecifics and influenced by environmental variables on the date of parturition. For elk, parturition events were most common during the morning crepuscular period and generally occurred later (i.e., closer to 12:00) when a relatively large proportion of the moon was illuminated. For mule deer, parturition events were most common during the diurnal period and generally occurred later (i.e., closer to 15:00) on cold, wet dates. Diel timing of parturition did not influence neonate survival, but larger datasets may be required to verify the apparent lack of influence. Although additional work could evaluate alternative variables that might affect parturition timing, our data provide an improved and finer scale understanding of reproductive ecology and phenology in ungulates.

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.

The missing fraction problem as an episodes of selection problem.

In evolutionary quantitative genetics, the missing fraction problem refers to a specific kind of bias in parameters estimated later in life that occurs when nonrandom subsets of phenotypes are missing from the population due to prior viability selection on correlated traits. The missing fraction problem thus arises when the following hold: (a) viability selection and (b) correlation between later-life traits and traits important for early-life survival. Although it is plausible that these conditions are widespread in wild populations, this problem has received little empirical attention. This may be natural: the problem could appear intractable, given that it is impossible to measure phenotypes of individuals that have previously died. However, it is not impossible to correctly measure lifetime selection, or correctly predict evolutionary trajectories, of later-life traits in the presence of the missing fraction. Two basic strategies are available. First, given phenotypic data on selected early life traits, well established but underused episodes of selection theory can yield correct values of evolutionary parameters throughout life. Second, when traits subjected to early-life viability selection are not known and/or measured, it is possible to use the genetic association of later-life traits with early-life viability to correctly infer important information about the consequences of prior viability selection for later-life traits. By carefully reviewing the basic nature of the missing fraction problem, and describing the tractable solutions to the problem, we hope that future studies will be able to be better designed to cope with the (likely pervasive) consequences of early-life viability selection.

An IL-10/DEL-1 axis supports granulopoiesis and survival from sepsis in early life

The limited reserves of neutrophils are implicated in the susceptibility to infection in neonates, however the regulation of neutrophil kinetics in infections in early life remains poorly understood. Here we show that the developmental endothelial locus (DEL-1) is elevated in neonates and is critical for survival from neonatal polymicrobial sepsis, by supporting emergency granulopoiesis. Septic DEL-1 deficient neonate mice display low numbers of myeloid-biased multipotent and granulocyte-macrophage progenitors in the bone marrow, resulting in neutropenia, exaggerated bacteremia, and increased mortality; defects that are rescued by DEL-1 administration. A high IL-10/IL-17A ratio, observed in newborn sepsis, sustains tissue DEL-1 expression, as IL-10 upregulates while IL-17 downregulates DEL-1. Consistently, serum DEL-1 and blood neutrophils are elevated in septic adult and neonate patients with high serum IL-10/IL-17A ratio, and mortality is lower in septic patients with high serum DEL-1. Therefore, IL-10/DEL-1 axis supports emergency granulopoiesis, prevents neutropenia and promotes sepsis survival in early life.

Interannual variation in survival of wild Atlantic salmon smolts through a dynamic estuarine habitat

AbstractMigration timing is critical for diadromous fish, especially for survival. Migration through fresh water and estuarine transitional waterbodies may be an important early life survival bottleneck through potential exposure to anthropogenic pressures and predators. Monitoring smolt movement and survival through riverine and estuarine habitats is important for identifying causes of smolt mortality and the potential for directing focused, mitigating management actions. Acoustic telemetry was used to track 186 Atlantic salmon smolts during migration from the river Boyne to the Irish Sea on the east coast of Ireland during 2019–2021. Migration success from release to sea entry that ranged from 47% to 81% was linked to biotic (predation) and abiotic effects (water flow and water temperature). Predation was associated with interannual variation in smolt survival, with 5.4% of smolts consumed by marine mammals and 26.3% lost to unknown fates. Our findings contribute to the understanding of predation on smolts and also how water temperature, flow and tidal phase can influence this critical life stage of Atlantic Salmon, a species in decline across its range.

Marine reserves promote cycles in fish populations on ecological and evolutionary time scales.

Marine reserves are considered essential for sustainable fisheries, although their effectiveness compared to traditional fisheries management is debated. The effect of marine reserves is mostly studied on short ecological time scales, whereas fisheries-induced evolution is a well-established consequence of harvesting. Using a size-structured population model for an exploited fish population of which individuals spend their early life stages in a nursery habitat, we show that marine reserves will shift the mode of population regulation from low size-selective survival late in life to low, early-life survival due to strong resource competition. This shift promotes the occurrence of rapid ecological cycles driven by density-dependent recruitment as well as much slower evolutionary cycles driven by selection for the optimal body to leave the nursery grounds, especially with larger marine reserves. The evolutionary changes increase harvesting yields in terms of total biomass but cause disproportionately large decreases in yields of larger, adult fish. Our findings highlight the importance of carefully considering the size of marine reserves and the individual life history of fish when managing eco-evolutionary marine systems to ensure both population persistence as well as stable fisheries yields.

How do fluctuating temperatures alter the cost of development?

Abstract Quantifying how variable temperature regimes affect energy expenditure during development is crucial for understanding how future thermal regimes may impact early life survival and population persistence. Developmental cost theory (DCT) suggests that there is an optimal temperature (Topt) that minimises energy expenditure during development (the ‘cost of development‘). Exposure to fluctuating temperatures around an average of Topt is anticipated to increase either development time or metabolic rate. As a result, embryos will rapidly deplete yolk reserves, and consequently hatch at a smaller size or with less residual yolk to support postnatal survival and growth. Here, we studied total embryonic energy expenditure (development time and rate of CO2 production) and conversion of yolk into tissue in common wall lizards (Podarcis muralis) under three incubation treatments anticipated, based on DCT, to increase the cost of development: no variance (Topt constant, 24°C), low variance (22°C–26°C) and high variance (18°C–30°C). As predicted, we found that increasing variance around Topt increased the cost of development, despite reducing time to hatching. As a consequence, embryos on average hatched with 59% lower residual yolk reserves under high variance versus the constant incubation temperature treatment. Our results highlight how the relative temperature sensitivities of development time and metabolic rate determine the cost of development, which in turn may predict the ability of egg‐laying ectotherms to persist in variable environments. We show that DCT can provide a mechanistic framework for understanding the widespread, but often seemingly idiosyncratic, effects of fluctuating incubation temperatures on hatchling tissue and residual yolk mass. Read the free Plain Language Summary for this article on the Journal blog.

Gadusol is a maternally provided sunscreen that protects fish embryos from DNA damage

Exposure to ultraviolet radiation (UVR) is harmful to living cells, leading organisms to evolve protective mechanisms against UVR-induced cellular damage and stress.1,2 UVR, particularly UVB (280-320nm), can damageproteins and DNA, leading to errors during DNA repair and replication. Excessive UVR can induce cellulardeath. Aquatic organisms face risk of UV exposure as biologically harmful levels of UVB can penetrate >10m in clear water.3 While melanin is the only known sunscreen in vertebrates, it often emerges late in embryonic development, rendering embryos of many species vulnerable during the earlier stages. Algae and microbes produce a class of sunscreening compounds known as mycosporine-like amino acids (MAAs).4 Fish eggs contain a similar compound called gadusol, whose role as a sunscreen has yet to be tested despite its discovery over 40 years ago.5 The recent finding that many vertebrate genomescontain a biosynthetic pathway for gadusol suggests that many fish may produce and use this molecule as a sunscreen.6 We generated a gadusol-deficient mutant zebrafish to investigate the role of gadusol in protecting fish embryos and larvae from UVR. Our results demonstrate that maternally provided gadusol is the primary sunscreen in embryonic and larval development, while melanin provides modest secondary protection. The gadusol biosynthetic pathway is retained in the vast majority of teleost genomes but is repeatedly lost in species whose young are no longer exposed to UVR. Our data demonstrate that gadusol is a maternally provided sunscreen that is critical for early-life survival in the most species-rich branch of the vertebrate phylogeny.

Position in the laying order has sex-specific consequences for reproductive success in adult black-headed gulls.

Mothers who produce multiple offspring within one reproductive attempt often allocate resources differentially; some maternally derived substances are preferentially allocated to last-produced offspring and others to first-produced offspring. The combined effect of these different allocation regimes on the overall fitness of offspring produced early or late in the sequence is not well understood, partly because production order is often coupled with birth order, making it difficult-to-separate effects of pre-natal maternal allocation from those of post-natal social environments. In addition, very little is known about the influence of laying order on fitness in later life. In this study, we used a semi-natural captive colony of black-headed gulls to test whether an offspring's position in the laying order affected its early-life survival and later-life reproductive success, independent of its hatching order. Later-laid eggs were less likely to hatch, but among those that did, survival to adulthood was greater than that of first-laid eggs. In adulthood, the laying order of females did not affect their likelihood of breeding in the colony, but male offspring hatched from last-laid eggs were significantly less likely to gain a breeding position than earlier-laid males. In contrast, later-laid female parents hatched lower proportions of their clutches than first-laid females, but hatching success was unrelated to the laying order of male parents. Our results indicate that gull mothers induce complex and sex-specific effects on both the early survival of their offspring and on long-term reproductive success through laying order effects among eggs of the same breeding attempt.

Life expectancy across countries: Convergence, divergence and fluctuations

We document the evolution of life expectancies around the world during 1960-2015 using graphical analysis, statistical decomposition of survival gains by age-groups and by measuring the contribution of each age-group to changes in the global and regional distributions of life expectancy at birth. We emphasize three findings. First, enormous gains in early-life survival have led to unconditional convergence in life expectancy at birth across countries while late-life longevity has diverged. Gains have been higher for females than males. Secondly, global and regional survival gains among the elderly, though smaller than among the young, have strongly influenced changes in country rankings of life expectancy at birth with the exception of sub-Saharan Africa. Country rankings for late-life survival have changed relatively more than for younger ages. Third, the divergence in survival gains among the elderly is related to disparities in healthcare access, driven in part by within- and between-country income inequality. While providing fresh insight into the uneven pace of health changes during the past half century, these results also highlight how policy can address the socio-economic and demographic consequences of aging.

Whole-genome sequencing of cryopreserved resources from French Large White pigs at two distinct sampling times reveals strong signatures of convergent and divergent selection between the dam and sire lines

BackgroundNumerous genomic scans for positive selection have been performed in livestock species within the last decade, but often a detailed characterization of the detected regions (gene or trait under selection, timing of selection events) is lacking. Cryopreserved resources stored in reproductive or DNA gene banks offer a great opportunity to improve this characterization by providing direct access to recent allele frequency dynamics, thereby differentiating between signatures from recent breeding objectives and those related to more ancient selection constraints. Improved characterization can also be achieved by using next-generation sequencing data, which helps narrowing the size of the detected regions while reducing the number of associated candidate genes.MethodsWe estimated genetic diversity and detected signatures of recent selection in French Large White pigs by sequencing the genomes of 36 animals from three distinct cryopreserved samples: two recent samples from dam (LWD) and sire (LWS) lines, which had diverged from 1995 and were selected under partly different objectives, and an older sample from 1977 prior to the divergence.ResultsFrench LWD and LWS lines have lost approximately 5% of the SNPs that segregated in the 1977 ancestral population. Thirty-eight genomic regions under recent selection were detected in these lines and the corresponding selection events were further classified as convergent between lines (18 regions), divergent between lines (10 regions), specific to the dam line (6 regions) or specific to the sire line (4 regions). Several biological functions were found to be significantly enriched among the genes included in these regions: body size, body weight and growth regardless of the category, early life survival and calcium metabolism more specifically in the signatures in the dam line and lipid and glycogen metabolism more specifically in the signatures in the sire line. Recent selection on IGF2 was confirmed and several other regions were linked to a single candidate gene (ARHGAP10, BMPR1B, GNA14, KATNA1, LPIN1, PKP1, PTH, SEMA3E or ZC3HAV1, among others).ConclusionsThese results illustrate that sequencing the genome of animals at several recent time points generates considerable insight into the traits, genes and variants under recent selection in a population. This approach could be applied to other livestock populations, e.g. by exploiting the rich biological resources stored in cryobanks.

Patterns, sources, and consequences of variation in age-specific vital rates: Insights from a long-term study of Weddell seals.

Variations in the reproductive and survival abilities of individuals within a population are ubiquitous in nature, key to individual fitness, and affect population dynamics, which leads to strong interest in understanding causes and consequences of vital-rate variation. For long-lived species, long-term studies of large samples of known-age individuals are ideal for evaluating vital-rate variation. A population of Weddell seals in Erebus Bay, Antarctica, has been studied each Austral spring since the 1960s. Since 1982, all newborns have been tagged each year and multiple capture-mark-recapture (CMR) surveys have been conducted annually. Over the past 20 years, a series of analyses have built on results of earlier research by taking advantage of steady improvements in the project's long-term CMR data and available analytical methods. Here, I summarize progress made on four major topics related to variation in age-specific vital rates for females: early-life survival and age at first reproduction, costs of reproduction, demographic buffering, and demographic senescence. Multistate modelling found that age at first reproduction varies widely (4-14 years of age) and identified contrasting influences of maternal age on survival and recruitment rates of offspring. Subsequent analyses of data for females after recruitment revealed costs of reproduction to both survival and future reproduction and provided strong evidence of demographic buffering. Recent results indicated that important levels of among-individual variation exist in vital rates and revealed contrasting patterns for senescence in reproduction and survival. Sources of variation in vital rates include age, reproductive state, year, and individual. The combination of luck and individual quality results in strong variation in individual fitness outcomes: ~80% of females born in the population produce no offspring, and the remaining 20% vary strongly in lifetime reproductive output (range: 1-23 pups). Further research is needed to identify the specific environmental conditions that lead to annual variation in vital rates and to better understand the origins of individual heterogeneity. Work is also needed to better quantify the relative roles of luck, maternal effects, and environmental conditions on variation in vital rates and to learn the importance of such variation to demographic performance of offspring and on overall population dynamics.

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.

Risk-taking neonates do not pay a survival cost in a free-ranging large mammal, the fallow deer (Dama dama).

Recent debate has focused on whether variation in personality primarily reflects variation in resource allocation or resource acquisition of individuals. These two mechanisms predict different relationships between personality and survival. If personality mainly reflects variation in resource allocation, then bold (i.e. risk-taking) individuals are expected to live shorter lives, whereas the opposite pattern is expected with resource acquisition. Here we studied the relationship between neonate personality and early-life survival in 269 juveniles of a population of fallow deer (Dama dama). We found that bolder individuals paid no apparent survival cost. Interestingly, among-individual differences in the physiological response at capture (heart rates, which covary with the behavioural response, i.e. latency to leave) were linked to survival, where individuals with lower heart rates when handled by humans had a higher probability of early-life survival. This suggests that bolder individuals may be of higher state than their shyer counterparts. As the first study linking neonate personality to survival in a free-ranging mammal, we provide novel insights into drivers behind early-life individual variation.

Impact of squid predation on juvenile fish survival

Predation is a major source of mortality during the early life stages of marine fishes; however, few studies have demonstrated its impact—especially that of squid predation—on survival processes. Here, we examined the feeding habits and predation impacts of swordtip squid on a major prey fish, juveniles of jack mackerel, in the East China Sea. Otoliths of the juveniles extracted from the squid stomach were used to reconstruct the age–length relationship and the growth trajectory of the consumed juveniles, and they were compared to those of juveniles collected with a net using a newly developed statistical framework. The juveniles consumed by squid had significantly shorter body lengths and smaller body sizes during the late larval and early juvenile stages than the netted juveniles, suggesting that smaller juveniles with slower growth rates have a higher probability to be selected. The body mass ratio of the predator squid to prey juveniles (predator–prey mass ratio, PPMR) ranged from 7 to 700, which was remarkably lower than the PPMR reported in various marine ecosystems based on analyses of fishes. Our findings demonstrate that squid predation can significantly impact the early life survival of fish and the trophodynamics in marine ecosystems.

Maternal food restriction during pregnancy affects offspring development and swimming performance in a placental live-bearing fish.

ABSTRACTHow pregnant mothers allocate limited resources to different biological functions such as maintenance, somatic growth, and reproduction can have profound implications for early life development and survival of offspring. Here, we examined the effects of maternal food restriction during pregnancy on offspring in the matrotrophic (i.e. mother-nourishment throughout gestation) live-bearing fish species Phalloptychus januarius (Poeciliidae). We fed pregnant females with either low or high food levels for 6 weeks and quantified the consequences for offspring size and body fat at birth and 1 week after birth. We further measured fast-start escape performance of offspring at birth, as well as swimming kinematics during prey capture at 0, 2 and 7 days after birth. We found that the length of maternal food restriction during pregnancy negatively affected offspring dry mass and lean dry mass at birth, as well as body fat gain during the first week after birth. Moreover, it impacted the locomotor performance of offspring during prey capture at birth and during the first week after birth. We did not observe an effect of food restriction on fast-start escape performance of offspring. Our study suggests that matrotrophic poeciliid fish are maladapted to unpredictably fluctuating resource environments, because sudden reductions in maternal food availability during pregnancy result in smaller offspring with slower postnatal body fat gain and an inhibition of postnatal improving swimming skills during feeding, potentially leading to lower competitive abilities after birth.

The association of obesity with thyroid carcinoma risk.

BackgroundThe prevalence of obesity and an increased incidence of thyroid carcinoma (TC) threaten public health in parallel on a global scale. Sufficient evidence supports excess body fatness in thyroid carcinogenesis, and the role and anthropometric markers of obesity have been causally associated with the rising risk of TC.MethodsA literature search was conducted in PubMed. Studies focused on the effect of obesity in TC.ResultsThis review mainly discusses the global incidence and prevalence of obesity‐related TC. We also review the role of obesity in TC and potential clinical strategies for obesity‐related TC.ConclusionsExcess body fatness in early life and TC survival initiate adverse effects later in life.

Self-tuition as an essential design feature of the brain.

We are curious by nature, particularly when young. Evolution has endowed our brain with an inbuilt obligation to educate itself. In this perspectives article, we posit that self-tuition is an evolved principle of vertebrate brain design that is reflected in its basic architecture and critical for its normal development. Self-tuition involves coordination between functionally distinct components of the brain, with one set of areas motivating exploration that leads to the experiences that train another set. We review key hypothalamic and telencephalic structures involved in this interplay, including their anatomical connections and placement within the segmental architecture of conserved forebrain circuits. We discuss the nature of educative behaviours motivated by the hypothalamus, innate stimulus biases, the relationship to survival in early life, and mechanisms by which telencephalic areas gradually accumulate knowledge. We argue that this aspect of brain function is of paramount importance for systems neuroscience, as it confers neural specialization and allows animals to attain far more sophisticated behaviours than would be possible through genetic mechanisms alone. Self-tuition is of particular importance in humans and other primates, whose large brains and complex social cognition rely critically on experience-based learning during a protracted childhood period.This article is part of the theme issue ‘Systems neuroscience through the lens of evolutionary theory’.