Somatic Maintenance Research Articles

The consequences of sea lamprey parasitism on lake trout energy budgets.

Parasitism is an energetically costly event for host species. Dynamic energy budget (DEB) theory describes the metabolic dynamics of an individual organism through its lifetime. Models derived from DEB theory specify how an organism converts food to reserves (maintenance-free energy available for metabolism) and allocates mobilized reserves to maintenance, growth (increase of structural body mass) and maturation or reproduction. DEB models thus provide a useful approach to describe the consequences of parasitism for host species. We developed a DEB model for siscowet lake trout and modeled the impact of sea lamprey parasitism on growth and reproduction using data collected from studies documenting the long-term effects following a non-lethal sea lamprey attack. The model was parameterized to reflect the changes in allocation of energy towards growth and reproduction observed in lake trout following sea lamprey parasitism and includes an estradiol module that describes the conversion of reproductive reserves to ovarian mass based on estradiol concentration. In our DEB model, parasitism increased somatic and maturity maintenance costs, reduced estradiol and decreased the estradiol-mediated conversion efficiency of reproductive reserves to ovarian mass. Muscle lipid composition of lake trout influenced energy mobilization from the reserve (efficiency of converting reserves allocated to reproduction into eggs) and reproductive efficiency. These model changes accurately reflect observed empirical changes to ovarian mass and growth. This model provides a plausible explanation of the energetic mechanisms that lead to skipped spawning following sea lamprey parasitism and could be used in population models to explore sublethal impacts of sea lamprey parasitism and other stressors on population dynamics.

Drosophila melanogaster females prioritise dietary sterols for producing viable eggs

Limiting calories or specific nutrients without malnutrition, otherwise known as dietary restriction (DR), has been shown to extend lifespan and reduce reproduction across a broad range of taxa. Our recent findings in Drosophila melanogaster show that supplementing flies on macronutrient-rich diets with additional cholesterol can extend lifespan to the same extent as DR, while also sustaining high egg production. Thus, DR may be beneficial for lifespan because it reduces egg production which in turn reduces the mother’s demand for sterols, thus supporting longer lifespan. It is also possible that mothers live longer and lay more eggs on high sterol diets because the diet triggers enhanced somatic maintenance and promotes egg production, but at the cost of diminished egg quality. To test this, we measured the viability of eggs and development of offspring from mothers fed either cholesterol-sufficient or cholesterol-limiting diets. We found that even when the mother’s diet was completely devoid of cholesterol, viable egg production persisted for ∼10 days. Furthermore, we show that sterol-supplemented flies with long lives lay eggs that have high viability and the same developmental potential as those laid by shorter lived mothers on sterol limiting diets. These findings suggest that offspring viability is not a hidden cost of lifespan extension seen in response to dietary sterol supplementation.

How do helpers slow senescence in a Tibetan cooperatively breeding bird?

AbstractSociality is known to be capable of slowing individual senescence, but it is unclear whether the effect differs for reproduction versus survival in a sex‐specific manner. Here we predict that social benefits are directed toward (1) somatic maintenance in harsh environments where high survival prospects of adults over young intensify the trade‐off between current and future reproduction, and (2) females that invest more in reproduction and have a greater marginal effect if their survival is improved by reducing the cost of reproduction. These two predictions are tested with cooperatively breeding Tibetan ground tits (Pseudopodoces humilis). Across the lifetime, both mothers and fathers with helpers did not differ in brood size at fledging from their counterparts without helpers. The presence of helpers reduced survival senescence of both parents, but mothers benefited more than fathers from receiving help. Consequently, the inherent sex difference in life span and along with lifetime reproductive success, as expressed in breeders of never‐receiving help, became no longer obvious. The model of social modulation for senescence should facilitate the persistence of cooperative breeding in challenging environments.

IRE-1 endoribonuclease activity declines early in C. elegans adulthood and is not rescued by reduced reproduction.

The proteome of a cell helps to define its functional specialization. Most proteins must be translated and properly folded to ensure their biological function, but with aging, animals lose their ability to maintain a correctly folded proteome. This leads to the accumulation of protein aggregates, decreased stress resistance, and the onset of age-related disorders. The unfolded protein response of the endoplasmic reticulum (UPRER) is a central protein quality control mechanism, the function of which is known to decline with age. Here, we show that age-related UPRER decline in Caenorhabditis elegans occurs at the onset of the reproductive period and is caused by a failure in IRE-1 endoribonuclease activities, affecting both the splicing of xbp-1 mRNA and regulated Ire1 dependent decay (RIDD) activity. Animals with a defect in germline development, previously shown to rescue the transcriptional activity of other stress responses during aging, do not show restored UPRER activation with age. This underlines the mechanistic difference between age-associated loss of UPRER activation and that of other stress responses in this system, and uncouples reproductive status from the activity of somatic maintenance pathways. These observations may aid in the development of strategies that aim to overcome the proteostasis decline observed with aging.

Multigenerational downregulation of insulin/IGF-1 signaling in adulthood improves lineage survival, reproduction, and fitness in Caenorhabditis elegans supporting the developmental theory of ageing.

Adulthood-only downregulation of insulin/IGF-1 signaling (IIS), an evolutionarily conserved pathway regulating resource allocation between somatic maintenance and reproduction, increases life span without fecundity cost in the nematode, Caenorhabditis elegans. However, long-term multigenerational effects of reduced IIS remain unexplored and are proposed to carry costs for offspring quality. To test this hypothesis, we ran a mutation accumulation (MA) experiment and downregulated IIS in half of the 400 MA lines by silencing daf-2 gene expression using RNA interference (RNAi) across 40 generations. Contrary to the prediction, adulthood-only daf-2 RNAi reduced extinction of MA lines both under UV-induced and spontaneous MA. Fitness of the surviving UV-induced MA lines was higher under daf-2 RNAi. Reduced IIS increased intergenerational F1 offspring fitness under UV stress but had no quantifiable transgenerational effects. Functional hrde-1 was required for the benefits of multigenerational daf-2 RNAi. Overall, we found net benefit to fitness from multigenerational reduction of IIS and the benefits became more apparent under stress. Because reduced daf-2 expression during development carries fitness costs, we suggest that our findings are best explained by the developmental theory of ageing, which maintains that the decline in the force of selection with age results in poorly regulated gene expression in adulthood.

Gap junctions mediate discrete regulatory steps during fly spermatogenesis.

Gametogenesis requires coordinated signaling between germ cells and somatic cells. We previously showed that Gap junction (GJ)-mediated soma-germline communication is essential for fly spermatogenesis. Specifically, the GJ protein Innexin4/Zero population growth (Zpg) is necessary for somatic and germline stem cell maintenance and differentiation. It remains unknown how GJ-mediated signals regulate spermatogenesis or whether the function of these signals is restricted to the earliest stages of spermatogenesis. Here we carried out comprehensive structure/function analysis of Zpg using insights obtained from the protein structure of innexins to design mutations aimed at selectively perturbing different regulatory regions as well as the channel pore of Zpg. We identify the roles of various regulatory sites in Zpg in the assembly and maintenance of GJs at the plasma membrane. Moreover, mutations designed to selectively disrupt, based on size and charge, the passage of cargos through the Zpg channel pore, blocked different stages of spermatogenesis. Mutations were identified that progressed through early germline and soma development, but exhibited defects in entry to meiosis or sperm individualisation, resulting in reduced fertility or sterility. Our work shows that specific signals that pass through GJs regulate the transition between different stages of gametogenesis.

Dietary restriction and ageing: Recent evolutionary perspectives

Dietary restriction (DR) represents one of the most robust interventions for extending lifespan. It is not known how DR increases lifespan. The prevailing evolutionary hypothesis suggests the DR response redirects metabolic resources towards somatic maintenance at the expense of investment in reproduction. Consequently, DR acts as a proximate mechanism which promotes a pro-longevity phenotype. This idea is known as resource reallocation. However, growing findings suggest this paradigm could be incomplete. It has been argued that during DR it is not always possible to identify a trade-off between reproduction and lifespan. It is also suggested the relationship between reproduction and somatic maintenance can be uncoupled by the removal or inclusion of specific nutrients. These findings have created an imperative to re-explore the nexus between DR and evolutionary theory. In this review I will address this evolutionary conundrum. My overarching objectives are fourfold: (1) to outline some of the evidence for and against resource reallocation; (2) to examine recent findings which have necessitated a theoretical re-evaluation of the link between life history theory and DR; (3) to present alternatives to the resource reallocation model; (4) to present emerging variables which potentially influence how DR effects evolutionary trade-offs.

Female reproduction and viral infection in a long-lived mammal.

For energetically limited organisms, life-history theory predicts trade-offs between reproductive effort and somatic maintenance. This is especially true of female mammals, for whom reproduction presents multifarious energetic and physiological demands. Here, we examine longitudinal changes in the gut virome (viral community) with respect to reproductive status in wild mature female chimpanzees Pan troglodytes schweinfurthii from two communities, Kanyawara and Ngogo, in Kibale National Park, Uganda. We used metagenomic methods to characterize viromes of individual chimpanzees while they were cycling, pregnant and lactating. Females from Kanyawara, whose territory abuts the park's boundary, had higher viral richness and loads (relative quantity of viral sequences) than females from Ngogo, whose territory is more energetically rich and located farther from large human settlements. Viral richness (total number of distinct viruses per sample) was higher when females were lactating than when cycling or pregnant. In pregnant females, viral richness increased with estimated day of gestation. Richness did not vary with age, in contrast to prior research showing increased viral abundance in older males from these same communities. Our results provide evidence of short-term physiological trade-offs between reproduction and infection, which are often hypothesized to constrain health in long-lived species.

Female-limited X chromosome evolution reveals that lifespan is mainly modulated by interlocus rather than intralocus sexual conflict

Sexual dimorphism in somatic investment may be shaped by two distinct forms of sexual conflict; under intralocus sexual conflict (IASC), males and females have different optimal levels of somatic investment but are constrained from reaching their respective optima by their shared genome, while under interlocus sexual conflict (IRSC), males and females have different optimal sexual strategies, which could have direct or indirect effects on levels of somatic investment. We investigated effects of IASC and IRSC on two aspects of somatic investment, immune defence strategies and longevity, using previously established female-limited experimental evolution lines in Drosophila melanogaster. We found little evidence for any effect of either type of sexual conflict on investment in the immune defence resistance or tolerance. Nor did we find convincing evidence that longevity is subject to IASC in this species. However, we did find evidence that increased female control over mating rate had important and opposite effects on longevity between the sexes. Specifically, females that had adapted to high levels of female control over mating had a longer lifespan when kept in mixed-sex groups, while males had shorter longevity, perhaps due to increased investment in post-copulatory sexual selection. These novel results show that female control over mating rates may have important and unexpected effects on patterns of somatic investment.Significance statementSexual conflict occurs between the two sexes over numerous life history traits, and it is complex to disentangle how these traits interact and affect each other. Here we use a long-term evolution experiment to investigate sexual dimorphism in somatic maintenance. We found no effect of feminising the X chromosome on female immune defence. However, we did find that increased female control over mating rate resulted in longer female lifespan, but reduced male lifespan, and that these effects were dependent on social context (isolated or in mixed-sex groups). Unlike previous studies on the effect of sexual conflict on longevity, our experiment did not manipulate environmental conditions nor the adult sex ratio, which is likely to reduce both pre- and post-copulatory sexual selection.

Somatic cell fate maintenance in mouse fetal testes via autocrine/paracrine action of AMH and activin B

Fate determination and maintenance of fetal testes in most mammals occur cell autonomously as a result of the action of key transcription factors in Sertoli cells. However, the cases of freemartin, where an XX twin develops testis structures under the influence of an XY twin, imply that hormonal factor(s) from the XY embryo contribute to sex reversal of the XX twin. Here we show that in mouse XY embryos, Sertoli cell-derived anti-Mullerian hormone (AMH) and activin B together maintain Sertoli cell identity. Sertoli cells in the gonadal poles of XY embryos lacking both AMH and activin B transdifferentiate into their female counterpart granulosa cells, leading to ovotestis formation. The ovotestes remain to adulthood and produce both sperm and oocytes, although there are few of the former and the latter fail to mature. Finally, the ability of XY mice to masculinize ovaries is lost in the absence of these two factors. These results provide insight into fate maintenance of fetal testes through the action of putative freemartin factors.

Cascading Effects of Conspecific Aggression on Oxidative Status and Telomere Length in Zebra Finches.

Living in social groups may exacerbate interindividual competition for territory, food, and mates, leading to stress and possible health consequences. Unfavorable social contexts have been shown to elevate glucocorticoid levels (often used as biomarkers of individual stress), but the downstream consequences of socially stressful environments are rarely explored. Our study experimentally tests the mechanistic links between social aggression, oxidative stress, and somatic maintenance in captive zebra finches (Taeniopygia guttata). Over 64 d, we measured the effects of aggression (received or emitted) on the individual oxidative status, body condition, and changes in relative telomere length (rTL) of birds living in high- and low-social-density conditions. Using path analyses, we found that birds living at high social density increased their aggressive behavior. Birds receiving the highest number of aggressions exhibited the strongest activation of antioxidant defenses and highest plasmatic levels of reactive oxygen metabolites. In turn, this prevented birds from maintaining or restoring telomere length between the beginning and the end of the experiment. Received aggression also had a direct negative effect on changes in rTL, unrelated to oxidative stress. In contrast, emitted aggression had no significant effect on individual oxidative stress or changes in rTL. Body condition did not appear to affect the physiological response to aggression or oxidative stress. At low density, we found trends that were similar to those at high density but nonsignificant. Our study sheds light on the causal chain linking the social environment and aggressive behavior to individual oxidative stress and telomere length. The long-term consequences of socially induced stress on fitness remain to be characterized.

Telomere dynamics in female Columbian ground squirrels: recovery after emergence and loss after reproduction.

Telomeres are specialized non-coding DNA sequences locatedat the end of chromosomesand that protect genetic information. Telomere loss over lifespan is generally viewed as a phenomenon associated with aging in animals. Recently, telomere elongation after hibernation has been described in several mammals. Whether this pattern is an adaptation to repair DNA damage caused during rewarming from torpor or if it coevolved as a mechanism to promote somatic maintenance in preparation for the upcoming reproductive effort remains unclear. In a longitudinal study measuring telomere length using buccal swabs, we tested if telomere elongation was related to reproductive success in wild adult female Columbian ground squirrels (Urocitellus columbianus) that were monitored from emergence from hibernation to the end of the reproductive season. We found three key results. First, female telomere length increased at the start of the breeding season, both in breeding and non-breeding individuals. Second, post-emergence telomere lengthening was unrelated to female future reproductive output. Third, telomere length decreased in breeding females during lactation, but remained stable in non-breeding females over a similar period. Within breeders, telomeres shortened more in females producing larger and heavier litters. We concluded that telomere lengthening after hibernation did not constrain immediate female reproductive capacities. It was more likely to be part of the body recovery process that takes place after hibernation. Telomere erosion that occurs after birth may constitute a physiological cost of female reproduction.

Large and expensive brain comes with a short lifespan: The relationship between brain size and longevity among fish taxa.

Vertebrates show substantial interspecific variation in brain size in relation to body mass. It has long been recognized that the evolution of large brains is associated with both costs and benefits, and it is their net benefit which should be favoured by natural selection. On one hand, the substantial energetic cost imposed by the maintenance of neural tissue is expected to compromise the energetic budget of organisms with large brains and their investment in other critical organs (expensive brain framework, EBF) or important physiological process, such as somatic maintenance and repair, thus accelerating ageing that shortens lifespan, as predicted by the disposable soma theory (DST). However, selection towards larger brain size can provide cognitive benefits (e.g., high behavioural flexibility) that may mitigate extrinsic mortality pressures, and thus may indirectly select for slower ageing that prolongs lifespan, as predicted by the cognitive buffer hypothesis (CBH). The relationship between longevity and brain size has been investigated to date only among terrestrial vertebrates, although the same selective forces acting on those species may also affect vertebrates living in aquatic habitats, such as fish. Thus, whether this evolutionary trade‐off for brain size and longevity exists on a large scale among fish clades remains to be addressed. In this study, using a global dataset of 407 fish species, I undertook the first phylogenetic test of the brain size/longevity relationship in aquatic vertebrate species. The study revealed a negative relationship between brain size and longevity among cartilaginous fish confirming EBF and DST. However, no pattern emerged among bony fish species. Among sharks and rays, the high metabolic cost of producing neural tissue transcends the cognitive benefits of evolving a larger brain. Consequently, my findings suggest that the cost of maintaining brain tissue is relatively higher in ectothermic species than in endothermic ones.

Intergenerational Inheritance of Altered Metabolism Phenotypes After Early‐life Stress in Caenorhabditis elegans

Environmental stress experienced during critical periods of animal development has been shown to impact adult phenotypes through changes in behavior or physiology. In humans, undernutrition in utero can lead to obesity and metabolic disorders in adulthood that can be inherited for two generations in the absence of the original stress. However, how particular stresses can result in tissue‐specific changes in target gene expression, and how that gene expression can be inherited, is not well understood. We have established Caenorhabditis elegans nematodes as a model system to investigate the molecular mechanisms that regulate environmental programming of gene expression. C. elegans larvae experiencing early‐life stress (starvation or crowding) may enter the stress resistant, developmentally arrested dauer stage. When environmental conditions improve, larvae will exit dauer and proceed with reproductive development (postdauers, PD). In previous work, we have shown using RNA‐Seq that hermaphrodites that experienced starvation‐induced dauer (PDStv) exhibited significant changes in gene expression compared to continuously fed animals (control, CON), most notably a downregulation of germline‐expressed genes and upregulation of genes with functions in fatty acid metabolism. These changes in gene expression correlated with production of fewer progeny and a decrease in stored intestinal lipids by Oil Red O (ORO) staining in PDStv adults compared to controls. The observed reduction in fecundity in PDStv hermaphrodites was dependent on functional Δ9‐desaturase genes, fat‐5, fat‐6, and fat‐7,as well as the DAF‐12/VDR steroid signaling pathway, indicating a connection between the starvation‐induced metabolism changes and fertility. Interestingly, embryos of PDStv hermaphrodites contained significantly more lipids compared to control embryos, suggesting that PDStv adults prioritize lipid production for reproduction rather than somatic maintenance after dauer exit. We next examined the lipid storage F1 and F2 generation adults using ORO staining, and found that F1 progeny of PDStv adults have significantly increased lipid storage compared to controls. This difference in lipid storage is reset in the F2 generation. Additionally, inheritance of the altered metabolism in F1 adults is dependent upon PRG‐1/PIWI and HRDE‐1/AGO siRNA pathways. In recent work, we are further investigating the connection between metabolism and fecundity of an animal that experienced early‐life stress. We examined the progeny number of PDStv adults that were cultivated on E. coli OP50 supplemented with different fatty acid molecules. We observed that supplementation with oleic acid (OA) resulted in a significant increase in progeny number compared to animals fed only E. coli, while other fatty acids resulted in no change or a decrease in progeny number. Furthermore, the OA‐dependent increase in progeny number required the Δ9‐desaturase FAT‐7, as well as the DAF‐12/VDR steroid signaling pathway, suggesting that OA may be modifying the starvation‐induced phenotypes of PDStv adults. Together, these results suggest that OA may be acting as a signaling molecule to modulate reproductive plasticity through regulation of the DAF‐12/VDR steroid signaling pathway in response to environmental conditions.

The comparative energetics of the cephalopods: they neither grow nor reproduce fast

The Add-my-Pet (AmP) collection of data on energetics and Dynamic Energy Budget (DEB) parameters currently contains 92 of the 800 extant species of cephalopods. Growth data, as reconstructed from statolith-, beak- or shell-readings, show a rather large scatter, whereas that from laboratory specimens with known age, does not. This implies that food availability varies under field conditions and/or age-determination is uncertain. We compare DEB parameter values and traits of cephalopods with those of other molluscs (Polyplacophora, Bivalvia, and Gastropoda). All cephalopods appear to start accelerating their metabolism at birth, quite few even up till puberty. As a consequence, length-at-age initially shows a clear up-curving at constant temperature and food, which is not clearly linked to morphological changes. They have a high acceleration factor, specific somatic maintenance, surface area-specific assimilation and maximum reserve density. The energy conductance, which controls reserve mobilisation, is typical for molluscs, and age at death is low. The investment into reproduction, in terms of specific offspring mass production per life span, is typical for molluscs. The negative effects that a short life span would have on reproductive output is compensated by a large allocation fraction to maturation or reproduction. Mass at birth is larger than that of gastropods, which, in turn, is much larger than that of bivalves and polyplacophorans. Cephalopod reproduction in terms of number of offspring per life time is, therefore, smaller than that of other molluscs. Although cephalopods are reputed to grow fast, gastropods grow equally fast per gram at maximum rate, while bivalves and polyplacophorans grow quite a bit slower. We conclude that 79% of the cephalopod species do not survive thinning of their populations in the long run, while this holds for some 20% of other animal species. This underscores their vulnerability for this type of harvesting.

Dynamic energy budget modeling of Atlantic surfclam, Spisula solidissima, under future ocean acidification and warming

A dynamic energy budget (DEB) model integrating pCO2 was used to describe ocean acidification (OA) effects on Atlantic surfclam, Spisula solidissima, bioenergetics. Effects of elevated pCO2 on ingestion and somatic maintenance costs were simulated, validated, and adapted in the DEB model based upon growth and biological rates acquired during a 12-week laboratory experiment. Temperature and pCO2 were projected for the next 100 years following the intergovernmental panel on climate change representative concentration pathways scenarios (2.6, 6.0, and 8.5) and used as forcing variables to project surfclam growth and reproduction. End-of-century water warming and acidification conditions resulted in simulated faster growth for young surfclams and more energy allocated to reproduction until the beginning of the 22nd century when a reduction in maximum shell length and energy allocated to reproduction was observed for the RCP 8.5 scenario.

Escargot controls somatic stem cell maintenance through the attenuation of the insulin receptor pathway in Drosophila.

SummaryAdult stem cells coordinate intrinsic and extrinsic, local and systemic, cues to maintain the proper balance between self-renewal and differentiation. However, the precise mechanisms stem cells use to integrate these signals remain elusive. Here, we show that Escargot (Esg), a member of the Snail family of transcription factors, regulates the maintenance of somatic cyst stem cells (CySCs) in the Drosophila testis by attenuating the activity of the pro-differentiation insulin receptor (InR) pathway. Esg positively regulates the expression of an antagonist of insulin signaling, ImpL2, while also attenuating the expression of InR. Furthermore, Esg-mediated repression of the InR pathway is required to suppress CySC loss in response to starvation. Given the conservation of Snail-family transcription factors, characterizing the mechanisms by which Esg regulates cell-fate decisions during homeostasis and a decline in nutrient availability is likely to provide insight into the metabolic regulation of stem cell behavior in other tissues and organisms.

The regulating effect of growth plasticity on the dynamics of structured populations

Plasticity is the extent to which life history processes such as growth and reproduction depend on the environment. Plasticity in individual growth varies widely between taxa. Nonetheless, little is known about the effect of plasticity in individual growth on the ecological dynamics of populations. In this article, we analyse a physiologically structured population model of a consumer population in which the individual growth rate can be varied between entirely plastic to entirely non-plastic. We derive this population level model from a dynamic energy budget model to ensure an accurate energetic coupling between ingestion, somatic maintenance, growth and reproduction within an individual. We show that the consumer population is either limited by adult fecundity or juvenile survival up to maturation, depending on the level of growth plasticity and the non-plastic individual growth rate. Under these two regimes, we also find two different types of population cycles which again arise due to fluctuation in, respectively, juvenile growth rate or adult fecundity. In the end, our model not only provides insight into the effects of growth plasticity on population dynamics, but also provides a link between the dynamics found in age- and size-structured models.

Selective Autophagy Receptor p62/SQSTM1, a Pivotal Player in Stress and Aging.

Efficient proteostasis is crucial for somatic maintenance, and its decline during aging leads to cellular dysfunction and disease. Selective autophagy is a form of autophagy mediated by receptors that target specific cargoes for degradation and is an essential process to maintain proteostasis. The protein Sequestosome 1 (p62/SQSTM1) is a classical selective autophagy receptor, but it also has roles in the ubiquitin-proteasome system, cellular metabolism, signaling, and apoptosis. p62 is best known for its role in clearing protein aggregates via aggrephagy, but it has recently emerged as a receptor for other forms of selective autophagy such as mitophagy and lipophagy. Notably, p62 has context-dependent impacts on organismal aging and turnover of p62 usually reflects active proteostasis. In this review, we highlight recent advances in understanding the role of p62 in coordinating the ubiquitin-proteasome system and autophagy. We also discuss positive and negative effects of p62 on proteostatic status and their implications on aging and neurodegeneration. Finally, we relate the link between defective p62 and diseases of aging and examine the utility of targeting this multifaceted protein to achieve proteostatic benefits.

A Life History Perspective on Athletes with Low Energy Availability.

The energy costs of athletic training can be substantial, and deficits arising from costs unmet by adequate energy intake, leading to a state of low energy availability, may adversely impact athlete health and performance. Life history theory is a branch of evolutionary theory that recognizes that the way the body uses energy-and responds to low energy availability-is an evolved trait. Energy is a finite resource that must be distributed throughout the body to simultaneously fuel all biological processes. When energy availability is low, insufficient energy may be available to equally support all processes. As energy used for one function cannot be used for others, energetic "trade-offs" will arise. Biological processes offering the greatest immediate survival value will be protected, even if this results in energy being diverted away from others, potentially leading to their downregulation. Athletes with low energy availability provide a useful model for anthropologists investigating the biological trade-offs that occur when energy is scarce, while the broader conceptual framework provided by life history theory may be useful to sport and exercise researchers who investigate the influence of low energy availability on athlete health and performance. The goals of this review are: (1) to describe the core tenets of life history theory; (2) consider trade-offs that might occur in athletes with low energy availability in the context of four broad biological areas: reproduction, somatic maintenance, growth, and immunity; and (3) use this evolutionary perspective to consider potential directions for future research.