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Schematic of OD and EGG hypotheses. (A) Early hominins, like living apes, have little difficulty in parturition; the neonatal brain is small relative to the pelvic outlet. (B) As hominin brain size expands, neonatal brain and pelvis size become tightly coupled. (C) The OD hypothesis proposes that further neonatal brain expansion is constrained by selection acting on pelvic width: the female pelvis cannot expand further because of selection on locomotor economy. (D) The EGG hypothesis proposes that further neonatal brain expansion is constrained by the limits of maternal energy supply: larger neonatal brain and body sizes would exceed the mother's capacity to provide energy to the fetus (Fig. 3).
Source publication
The classic anthropological hypothesis known as the "obstetrical dilemma" is a well-known explanation for human altriciality, a condition that has significant implications for human social and behavioral evolution. The hypothesis holds that antagonistic selection for a large neonatal brain and a narrow, bipedal-adapted birth canal poses a problem f...
Citations
... Since our ancestors were already bipedal when rapid pulses in brain size increase occurred (Gómez-Robles et al., 2017), there was an upper limit for when babies could be born (Washburn, 1960;Rosenberg & Trevathan, 1995;Dunsworth & Eccleston, 2015;Haeusler et al., 2021;Webb et al., 2024). In addition, in modern humans, the mother's own metabolism is unable to transform enough energy to support any further intrauterine (brain) growth (Dunsworth et al., 2012;Thurber et al., 2019). Both factors clearly prevent human infants from being born later. ...
... This evidence from the paleontological record makes it unlikely that bipedality was the feature that triggered the feedback loop of Figure 1, although it contributed to earlier birth as brain size increased. Likewise, maternal metabolic constraints are unlikely triggers because they only became limiting once brains already had substantially increased (Dunsworth et al., 2012) and because the maternal maximum sustained metabolic scope is reached during lactation rather than during gestation (Thurber et al., 2019). ...
Unlike any other great ape, humans give birth to large, secondarily altricial babies, show precocial social development, have bigger brains that require a long maturation period, and engage in cooperative breeding (CB). These traits, which characterize the human adaptive complex, are intricately linked and must have mutually reinforced each other over evolutionary time. Here, we use recent evidence from paleontology, developmental psychology, and pediatrics, complemented with comparative analyses to ask what may have triggered this coevolutionary feedback loop: bipedality, direct selection on altriciality, a higher-quality diet, or cooperative breeding. An early adoption of extensive allomaternal care during human evolution, i.e. the CB-first model, best accommodates the available data. In particular, CB was a catalyst enabling further increases in brain size, because even though larger brains slow down life history and neurodevelopment and thus lead to a demographic dilemma, CB enabled the necessary increase in birth rates.
... Additionally, human infants have accelerated brain growth outside the womb, known as secondary altriciality, where human brains are 30% less developed than other primates when birthed [22,23]. The demands of the size of the womb favored fetuses in earlier development in order to fit through the narrow birth canal; therefore, a fetus's head grows significantly after birth [23]. In primates in general and humans in particular, pelvis shape is sexually dimorphic and changes over time according to estradiol levels; the size of the pelvis changes to "prime" for birthing when a female reaches reproductive age [18]. ...
... The human fetus, in relation to its mother's weight, is twice as large compared to primates of similar size, making it an outlier for female human capacity. Additionally, human infants have accelerated brain growth outside the womb, known as secondary altriciality, where human brains are 30% less developed than other primates when birthed [22,23]. The demands of the size of the womb favored fetuses in earlier development in order to fit through the narrow birth canal; therefore, a fetus's head grows significantly after birth [23]. ...
... Additionally, human infants have accelerated brain growth outside the womb, known as secondary altriciality, where human brains are 30% less developed than other primates when birthed [22,23]. The demands of the size of the womb favored fetuses in earlier development in order to fit through the narrow birth canal; therefore, a fetus's head grows significantly after birth [23]. ...
The female pelvis is often evolutionarily described as a compromise to accommodate the birthing process and bipedalism. This compromise puts a mother and baby at risk of fetopelvic disproportion, the mismatch between the size of the fetus and that of the mother’s pelvis, impacting the ease with which the vaginal birthing process occurs. Obstructed labor, commonly caused by fetopelvic disproportion, is a leading cause of maternal mortality and morbidity and has serious medical sequelae for the fetus. In this review, this evolutionary aspect of fetopelvic disproportion is reconsidered within a broader sociocultural and environmental approach related to a change of paradigm from a more reductionist Neo-Darwinist to a more encompassing Extended Evolutionary Synthesis view. The review explores a more comprehensive understanding of several factors related to fetopelvic disproportion, including socioeconomic factors and ethnic disparities among individuals that might lead to a higher likelihood of obstructed labor and maternal and fetal morbidity and mortality.
... The timing of events in the lifetimes of organisms is critical, and various genetic mechanisms have evolved to track the passage of time at various scales [15][16][17][18][19]. Developmental sequences of a given species map out with regularity across time, and important changes often relate to changes in timing. Homo sapiens, for example, in comparison to other apes, are characterized by delayed rates of sexual maturation, long childhood dependency, and differential rates of growth (e.g., brain size, body size) and development (shape) across the lifespan [20,21]. Other changes in timing and sequence (e.g., humans, uniquely among primates, acquire their canines early, roughly at the same time as their incisors- [22,23] are likely the product of important adaptive transitions. ...
The propensity of humans and non-human animals to discount future returns for short-term benefits is well established. This contrasts with the ability of organisms to unfold complex developmental sequences over months or years efficiently. Research has focused on various descriptive and predictive parameters of ‘temporal discounting’ in behavior, and researchers have proposed models to explain temporal preference in terms of fitness-maximizing outcomes. Still, the underlying ultimate cause of this phenomenon has not been deeply explored across taxa. Here, we propose an ultimate (i.e., evolutionary) causal explanation for the selection of temporal discounting largely conserved across taxa. We propose that preference for a short-term reward (e.g., heightened impulsivity) often is less than optimal and likely is the product of constraints imposed on natural selection with respect to predicting events in a temporal framework in the context of future uncertainty. Using a simple Newtonian model for time across a fitness landscape in which movement by organisms is only possible in one direction, we examine several factors that influence the ability of an organism to choose a distant reward over a more temporally proximate reward: including the temporal distance of the far reward, the relative value of the distant reward, and the effect of uncertainty about the value and presence of the distant reward. Our results indicate that an organism may choose a more distant reward, but only if it is not too far into the future and has a substantially higher-value fitness payoff relative to the short-term reward. Notably, any uncertainty about the distant reward made it extremely unlikely for an organism to choose the delayed reward strategy compared to choosing a closer reward, even if the distant reward had a much higher payoff because events that are uncertain are only partially visible to natural selection pressures. The results help explain why natural selection is constrained to promote more optimal behavioral strategies and why it has difficulty selecting a distant reward over a lower-value short-term reward. The degree of uncertainty is an especially salient ecological variable in promoting and preferencing short-term behavioral strategies across taxa. These results further help illustrate why, from an ultimate causal perspective, human and non-human taxa have difficulty making more optimal long-term decisions.
... Even chimpanzees, our nearest evolutionary cousins, have brains at birth that exceed 40% of the adult brain size [2], whereas the brains in human newborn brains are less than 30% of the adult size. Scientists estimate that for a human infant's brain to develop similarly to that of a baby chimpanzee's, gestation would need to last between 18 and 21 months [3]. However, extended pregnancy is not feasible because the infant's head is too large to pass through the birth canal. ...
Brain development is an extremely complex and essential biological process that begins at the start of life and continues throughout an individual’s lifespan [...]
... Fetal growth restriction is often due to placental dysfunction associated with reduced activity of the glutamine and glutamate transporter (McIntyre et al. 2020). During normal pregnancy, maternal metabolic rate doubles at 6 months of gestation and does not increase further, even in populations where mothers do physical work during pregnancy (Dunsworth et al. 2012). In other words, aside from anatomical constraints (i.e., an evolved trade-o between maternal pelvis size and fetal head circumference), it could well be that the fetal energy demand requires the antedating of human birth as it seems the maternal body cannot provide su cient energy beyond 40 weeks of gestation (Campbell 2010;Dunsworth et al. 2012). ...
... During normal pregnancy, maternal metabolic rate doubles at 6 months of gestation and does not increase further, even in populations where mothers do physical work during pregnancy (Dunsworth et al. 2012). In other words, aside from anatomical constraints (i.e., an evolved trade-o between maternal pelvis size and fetal head circumference), it could well be that the fetal energy demand requires the antedating of human birth as it seems the maternal body cannot provide su cient energy beyond 40 weeks of gestation (Campbell 2010;Dunsworth et al. 2012). This interpretation p. 464 ...
Neuropsychopharmacology is the field of medicine that deals with the neural mechanisms explaining how neurotropic molecules affect brain function. The mechanisms involved include neurological processes, such as the functioning of sensory and motor systems, as well as the functioning of the mind (ie, the study of cognition, emotion, and behavior) in relation to the action of neurotransmitters, neuromodulators, and psychotropic drugs. 1 Accordingly, neuropsychopharmacology draws on concepts and knowledge from the fields of neuroanatomy, neuropathology, pharmacokinetics, and neuroscience. Neuropsychopharmacology is closely related to psychopharmacology but adds to the latter a more in-depth analysis of biochemical processes contributing to the modulation of receptor activity that are relevant for the understanding and treatment of psychiatric and neurological conditions.
In recent years, new task forces have been formed with the aim of replacing disorderor disease-driven nomenclature (eg, antidepressants, antipsychotics, antiepileptics, etc.) with a classification of drugs based on their pharmacological properties. This change helps shift focus from symptoms to the understanding of mechanisms and from disease (entity) to treatments. In addition, a new nomenclature may improve the integration of new findings from neuroscience research. More details on the goals of the task forces can be found on the homepages of the American College of Neuropsychopharmacology (ACNP), the European College of Neuropsychopharmacology, the International Union of Basic and Clinical Pharmacology, and others.
... The onset of labor likely relies on various overlapping gestational clocks and redundant signaling mechanisms (22,64,65). Several mechanisms influence cervical ripening and uterine activation (66,67), including corticotropin-releasing hormone (68), progesterone receptor isoform expression (69), placental cell free DNA release (70), gasotransmitters (71,72), epigenetic (73), and metabolic signals (22,23,74,75). Research in both broad metabolomics and specific analytes might provide opportunities to identify predictive preterm birth biomarkers. The anti-inflammatory and tocolytic effects of adiponectin could contribute to pregnancy maintenance (12)(13)(14)23). ...
Context
Adiponectin is a potent uterine tocolytic that decreases with gestational age, suggesting it could be a maternal metabolic quiescence factor. Maternal stress can influence preterm birth risk, and adiponectin levels may be stress responsive.
Objective
We characterized associations between adiponectin and glucocorticoids with preterm birth and modeled their predictive utility. We hypothesized maternal plasma adiponectin and cortisol are inversely related and lower adiponectin and higher cortisol associate with preterm birth.
Methods
We performed a nested case–control study using biobanked fasting maternal plasma. We included low-risk singleton pregnancies, and matched 1:3 (16 preterm, 46 term). We quantified high molecular weight (HMW), low molecular weight (LMW), and total adiponectin using an enzyme-linked immunosorbent assay. We validated a high-performance liquid chromatography-tandem mass spectrometry serum assay for use in plasma, to simultaneously measure cortisol, cortisone, and 5 related steroid hormones. We used linear/logistic regression to compare group means and machine learning for predictive modeling.
Results
The preterm group had lower mean LMW adiponectin (3.07 μg/mL vs 3.81 μg/mL at 15 weeks (w) 0 days (d), P = .045) and higher mean cortisone (34.4 ng/mL vs 29.0 ng/mL at 15w0d, P = .031). The preterm group had lower cortisol to cortisone and lower LMW adiponectin to cortisol ratios. We found HMW adiponectin, cortisol to cortisone ratio, cortisone, maternal height, age, and prepregnancy body mass index most strongly predicted preterm birth (area under the receiver operator curve = 0.8167). In secondary analyses, we assessed biomarker associations with maternal self-reported psychosocial stress. Lower perceived stress was associated with a steeper change in cortisone in the term group.
Conclusion
Overall, metabolic and stress biomarkers are associated with preterm birth in this healthy cohort. We identify a possible mechanistic link between maternal stress and metabolism for pregnancy maintenance.
... Fetal growth restriction is often due to placental dysfunction associated with reduced activity of the glutamine and glutamate transporter (McIntyre et al. 2020). During normal pregnancy, maternal metabolic rate doubles at 6 months of gestation and does not increase further, even in populations where mothers do physical work during pregnancy (Dunsworth et al. 2012). In other words, aside from anatomical constraints (i.e., an evolved trade-o between maternal pelvis size and fetal head circumference), it could well be that the fetal energy demand requires the antedating of human birth as it seems the maternal body cannot provide su cient energy beyond 40 weeks of gestation (Campbell 2010;Dunsworth et al. 2012). ...
... During normal pregnancy, maternal metabolic rate doubles at 6 months of gestation and does not increase further, even in populations where mothers do physical work during pregnancy (Dunsworth et al. 2012). In other words, aside from anatomical constraints (i.e., an evolved trade-o between maternal pelvis size and fetal head circumference), it could well be that the fetal energy demand requires the antedating of human birth as it seems the maternal body cannot provide su cient energy beyond 40 weeks of gestation (Campbell 2010;Dunsworth et al. 2012). This interpretation p. 464 ...
This book provides a cutting-edge overview of emotion science from an evolutionary perspective. Part 1 outlines different ways of approaching the study of emotion; Part 2 covers specific emotions from an evolutionary perspective; Part 3 discusses the role of emotions in a variety of life domains; and Part 4 explores the relationship between emotions and psychological disorders. Experts from a number of different disciplines—psychology, biology, anthropology, psychiatry, and more—tackle a variety of “how” (proximate) and “why” (ultimate) questions about the function of emotions in humans and nonhuman animals, how emotions work, and their place in human life. This volume documents the explosion of knowledge in emotion science over the last few decades, outlines important areas of future research, and highlights key questions that have yet to be answered.
... This raises interesting questions, especially in the light of recent studies showing that not only anatomical and morphological limitations (e.g., pelvic dimensions), but also energetic physiological constraints may directly regulate gestation length in mammals, including nonhuman primates and humans (Dunsworth et al. 2012;cf. Kurismaa 2021a). ...
... However, in the light of physiological work and motor responses may stimulate growth and development in the organism via both the first and the second type of anabolic processes (Arshavsky 1972(Arshavsky , 1982. and mechanistic considerations (Dunsworth et al. 2012;Jackson et al. 2014;Pontzer 2018) such effects do appear likely and might have important evolutionary implications. ...
The problems of organismal agency and phenotypic plasticity present significant interest for modern developmental and evolutionary biology, as well as comparative and biosemiotic approaches. At the same time, the question of how behavioural and other proximal phenotypic factors may potentially drive developmental and evolutionary variation remains open, particularly in relation to life-history and allometric theory (where the issue of agency has been seldom explored). To fill these gaps, this chapter revisits the anti-entropic (negentropic) approach to ontogeny developed by I.A. Arshavsky (1903–1996) and his school. Within this tradition, diverse developmental processes and organisms were studied in order to understand how biological agency and phenotypic plasticity can be interrelated and together affect the formation and integration of biological traits – including the remarkable physiological and morphological features distinguishing primarily altricial (immaturely born) from primarily precocial (maturely born) eutherians. This chapter revisits these concepts and results in the light of current research. In particular, that Arshavsky’s non-equilibrium approach may still help to frame new questions and integrative concepts is shown with respect to certain unresolved problems of metabolic scaling, including the apparent biophysical paradox of increased work capacity and bioenergetic reserves in larger/more precocial organisms. Finally, we shall also consider a novel anti-entropic hypothesis regarding possible agential origins of the prolonged gestation and reduced offspring numbers in such animals, which may have a variety of implications for current work in biology and biosemiotics.
... His interpretation of this 'obstetrical dilemma' was that it resulted in human offspring being born at a relatively early stage of development. Subsequent work has shown that our gestation is not short compared to other apes [54,55], while there is discussion over whether maternal energetic limits might also explain the typical duration of human pregnancy [55,56]. Nonetheless, maternal pelvic dimensions may still be subject to evolutionary constraint [57]. ...
... His interpretation of this 'obstetrical dilemma' was that it resulted in human offspring being born at a relatively early stage of development. Subsequent work has shown that our gestation is not short compared to other apes [54,55], while there is discussion over whether maternal energetic limits might also explain the typical duration of human pregnancy [55,56]. Nonetheless, maternal pelvic dimensions may still be subject to evolutionary constraint [57]. ...
In uncomplicated pregnancies, birthweight is inversely associated with adult non-communicable disease (NCD) risk. One proposed mechanism is maternal malnutrition during pregnancy. Another explanation is that shared genes link birthweight with NCDs. Both hypotheses are supported, but evolutionary perspectives address only the environmental pathway. We propose that genetic and environmental associations of birthweight with NCD risk reflect coordinated regulatory systems between mother and fetus, that evolved to reduce risks of obstructed labour. First, the fetus must tailor its growth to maternal metabolic signals, as it cannot predict the size of the birth canal from its own genome. Second, we predict that maternal alleles that promote placental nutrient supply have been selected to constrain fetal growth and gestation length when fetally expressed. Conversely, maternal alleles that increase birth canal size have been selected to promote fetal growth and gestation when fetally expressed. Evidence supports these hypotheses. These regulatory mechanisms may have undergone powerful selection as hominin neonates evolved larger size and encephalisation, since every mother is at risk of gestating a baby excessive for her pelvis. Our perspective can explain the inverse association of birthweight with NCD risk across most of the birthweight range: any constraint of birthweight, through plastic or genetic mechanisms, may reduce the capacity for homeostasis and increase NCD susceptibility. However, maternal obesity and diabetes can overwhelm this coordination system, challenging vaginal delivery while increasing offspring NCD risk. We argue that selection on viable vaginal delivery played an over-arching role in shaping the association of birthweight with NCD risk.
... This condition has been labelled 'secondary altriciality', in contrast to the precociality of other primates, but also to distinguish it from true altriciality, the primitive condition for mammals [4]. However, whether secondary altriciality is due to pelvic constraints [5] or maternal metabolic limitations [6] remains unclear. The former hypothesis attributes secondary altriciality to an evolutionary trade-off between natural selection for a sufficiently large birth canal in females and a biomechanically efficient pelvis with a short sacroiliac-to-hip joint distance adapted for bipedal locomotion in both sexes [7][8][9][10]. ...
... The most comprehensive critique of the obstetrical dilemma to date is offered by the 'Energetics of Gestation and Growth (EGG) hypothesis'. It not only questions that difficult birth was caused by pelvic adaptations to bipedal locomotion but also provides an alternative explanation for secondary altriciality, thus countering two of the central pillars of the obstetrical dilemma hypothesis [6,19]. In analogy to the constrained model of total energy expenditure (TEE) for physical activity [20][21][22][23], the EGG hypothesis posits that the increasing energy demands of the pregnant mother approach a plateau towards the end of the third trimester, suggesting the presence of a 'metabolic ceiling' or threshold. ...
... Yet, the EGG hypothesis also lacks an explanation for the high prevalence of birth difficulties and the marked degree of pelvic sexual dimorphism typical of all modern human populations. [6]). The additional maternal energy requirements are based on the study of Goldberg et al. [24] and seem to plateau in the third trimester, thus approaching a theoretical maximum sustained metabolic scope, which was suggested to lie between 2.04 × BMR (inferred from Fig. 3 in Dunsworth et al. [6]) and 2.1 × BMR. ...
A hallmark of modern humans is that our newborns are neurologically immature compared to other primates. It is disputed whether this so-called secondary altriciality evolved due to remodelling of the pelvis associated with bipedal locomotion, as suggested by the obstetrical dilemma hypothesis, or from maternal energetic limitations during pregnancy. Specifically, the ‘Energetics of Gestation and Growth’ (EGG) hypothesis posits that birth is initiated when foetal energy requirements exceed the maximum sustained maternal metabolic rate during pregnancy at around 2.1 × basal metabolic rate (BMR) of the non-pregnant, non-lactating condition (NPNL). However, the metabolic threshold argued under the EGG framework is derived from one study with a small sample size of only 12 women from the UK. Accordingly, we performed a meta-analysis of all published studies on metabolic scopes during pregnancy to better account for variability. After excluding 3 studies with methodological issues, a total of 12 studies with 303 women from 5 high- and 3 low-income countries were analysed. On average, pregnancy was found to be less metabolically challenging than previously suggested. The studies revealed substantial variation in metabolic scope during pregnancy, which was not reflected by variation in birth timing. Further, in a third of the studies, the metabolic rates exceeded 2.1 × BMRNPNL. Our simulation of foetal energy requirements demonstrated that this metabolic threshold of 2.1 × BMRNPNL cannot realistically be crossed by the foetus around the time of birth. These findings imply that metabolic constraints are not the main limiting factor dictating gestation length.
