There is an obstetrical dilemma: Misconceptions about the evolution of human childbirth and pelvic form

Compared to other primates, modern humans face high rates of maternal and neonatal morbidity and mortality during childbirth. Since the early 20th century, this “difficulty” of human parturition has prompted numerous evolutionary explanations, typically assuming antagonistic selective forces acting on maternal and fetal traits, which has been termed the “obstetrical dilemma.” Recently, there has been a growing tendency among some anthropologists to question the difficulty of human childbirth and its evolutionary origin in an antagonistic selective regime. Partly, this stems from the motivation to combat increasing pathologization and overmedicalization of childbirth in industrialized countries. Some authors have argued that there is no obstetrical dilemma at all, and that the difficulty of childbirth mainly results from modern lifestyles and inappropriate and patriarchal obstetric practices. The failure of some studies to identify biomechanical and metabolic constraints on pelvic dimensions is sometimes interpreted as empirical support for discarding an obstetrical dilemma. Here we explain why these points are important but do not invalidate evolutionary explanations of human childbirth. We present robust empirical evidence and solid evolutionary theory supporting an obstetrical dilemma, yet one that is much more complex than originally conceived in the 20th century. We argue that evolutionary research does not hinder appropriate midwifery and obstetric care, nor does it promote negative views of female bodies. Understanding the evolutionary entanglement of biological and sociocultural factors underlying human childbirth can help us to understand individual variation in the risk factors of obstructed labor, and thus can contribute to more individualized maternal care.     

The obstetrical dilemma hypothesis: there's life in the old dog yet

The term ‘obstetrical dilemma’ was coined by Washburn in 1960 to describe the trade-off between selection for a larger birth canal, permitting successful passage of a big-brained human neonate, and the smaller pelvic dimensions required for bipedal locomotion. His suggested solution to these antagonistic pressures was to give birth prematurely, explaining the unusual degree of neurological and physical immaturity, or secondary altriciality, observed in human infants. This proposed trade-off has traditionally been offered as the predominant evolutionary explanation for why human childbirth is so challenging, and inherently risky, compared to that of other primates. This perceived difficulty is likely due to the tight fit of fetal to maternal pelvic dimensions along with the convoluted shape of the birth canal and a comparatively low degree of ligamentous flexibility. Although the ideas combined under the obstetrical dilemma hypothesis originated almost a century ago, they have received renewed attention and empirical scrutiny in the last decade, with some researchers advocating complete rejection of the hypothesis and its assumptions. However, the hypothesis is complex because it presently captures several, mutually non-exclusive ideas: (i) there is an evolutionary trade-off resulting from opposing selection pressures on the pelvis; (ii) selection favouring a narrow pelvis specifically derives from bipedalism; (iii) human neonates are secondarily altricial because they are born relatively immature to ensure that they fit through the maternal bony pelvis; (iv) as a corollary to the asymmetric selection pressure for a spacious birth canal in females, humans evolved pronounced sexual dimorphism of pelvic shape. Recently, the hypothesis has been challenged on both empirical and theoretical grounds. Here, we appraise the original ideas captured under the ‘obstetrical dilemma’ and their subsequent evolution. We also evaluate complementary and alternative explanations for a tight fetopelvic fit and obstructed labour, including ecological factors related to nutrition and thermoregulation, constraints imposed by the stability of the pelvic floor or by maternal and fetal metabolism, the energetics of bipedalism, and variability in pelvic shape. This reveals that human childbirth is affected by a complex combination of evolutionary, ecological, and biocultural factors, which variably constrain maternal pelvic form and fetal growth. Our review demonstrates that it is unwarranted to reject the obstetrical dilemma hypothesis entirely because several of its fundamental assumptions have not been successfully discounted despite claims to the contrary. As such, the obstetrical dilemma remains a tenable hypothesis that can be used productively to guide evolutionary research.     

A Wider Pelvis Does Not Increase Locomotor Cost in Humans,with Implications for the Evolution of Childbirth

The shape of the human female pelvis is thought to reflect an evolutionary trade-off between two competing demands: a pelvis wide enough to permit the birth of large-brained infants, and narrow enough for efficient bipedal locomotion. This trade-off, known as the obstetrical dilemma, is invoked to explain the relative difficulty of human childbirth and differences in locomotor performance between men and women. The basis for the obstetrical dilemma is a standard static biomechanical model that predicts wider pelves in females increase the metabolic cost of locomotion by decreasing the effective mechanical advantage of the hip abductor muscles for pelvic stabilization during the single-leg support phase of walking and running, requiring these muscles to produce more force. Here we experimentally test this model against a more accurate dynamic model of hip abductor mechanics in men and women. The results show that pelvic width does not predict hip abductor mechanics or locomotor cost in either women or men, and that women and men are equally efficient at both walking and running. Since a wider birth canal does not increase a woman’s locomotor cost, and because selection for successful birthing must be strong, other factors affecting maternal pelvic and fetal size should be investigated in order to help explain the prevalence of birth complications caused by a neonate too large to fit through the birth canal.     

Between Scylla and Charybdis: renegotiating resolution of the ‘obstetric dilemma’ in response to ecological change

Hominin evolution saw the emergence of two traits—bipedality and encephalization—that are fundamentally linked because the fetal head must pass through the maternal pelvis at birth, a scenario termed the ‘obstetric dilemma’. While adaptive explanations for bipedality and large brains address adult phenotype, it is brain and pelvic growth that are subject to the obstetric dilemma. Many contemporary populations experience substantial maternal and perinatal morbidity/mortality from obstructed labour, yet there is increasing recognition that the obstetric dilemma is not fixed and is affected by ecological change. Ecological trends may affect growth of the pelvis and offspring brain to different extents, while the two traits also differ by a generation in the timing of their exposure. Two key questions arise: how can the fit between the maternal pelvis and the offspring brain be ‘renegotiated’ as the environment changes, and what nutritional signals regulate this process? I argue that the potential for maternal size to change across generations precludes birthweight being under strong genetic influence. Instead, fetal growth tracks maternal phenotype, which buffers short-term ecological perturbations. Nevertheless, rapid changes in nutritional supply between generations can generate antagonistic influences on maternal and offspring traits, increasing the risk of obstructed labour.     

Divergent patterns of integration and reduced constraint in the human hip and the origins of bipedalism

When compared to other hominids--great apes including humans--the human pelvis reveals a fundamental reorganization of bony morphology comprised of multiple trait-level changes, many of which are associated with bipedal locomotion. Establishing how patterns of integration--correlations and covariances among traits--within the pelvis have evolved in concert with morphology is essential to explaining this evolutionary transition because integration may facilitate or constrain morphological evolution. Here, we show that the human hip bone has significantly lower levels of integration and constraint overall when compared to other hominids, that the focus of these changes is on traits hypothesized to play major functional roles in bipedalism, and we provide evidence that the human hip was reintegrated in a pattern distinct from other members of this group. Additionally, the evolutionary transition from a nonhuman great ape-like to human hip bone morphology was significantly easier to traverse using the human integration pattern in each comparison, which suggests hominin patterns may have evolved to facilitate this transition. Our results suggest natural selection for bipedalism broke down earlier hominid integration patterns, allowing relevant traits to respond to separate selection pressures to a greater extent than was previously possible, and reintegrated traits in a way that could have facilitated evolution along the vector specifying ancestral hominid and hominin morphological differences.     

Adaptive Social Learning Strategies in Temporally and Spatially Varying Environments

Long before the origins of agriculture human ancestors had expanded across the globe into an immense variety of environments, from Australian deserts to Siberian tundra. Survival in these environments did not principally depend on genetic adaptations, but instead on evolved learning strategies that permitted the assembly of locally adaptive behavioral repertoires. To develop hypotheses about these learning strategies, we have modeled the evolution of learning strategies to assess what conditions and constraints favor which kinds of strategies. To build on prior work, we focus on clarifying how spatial variability, temporal variability, and the number of cultural traits influence the evolution of four types of strategies: (1) individual learning, (2) unbiased social learning, (3) payoff-biased social learning, and (4) conformist transmission. Using a combination of analytic and simulation methods, we show that spatial??but not temporal??variation strongly favors the emergence of conformist transmission. This effect intensifies when migration rates are relatively high and individual learning is costly. We also show that increasing the number of cultural traits above two favors the evolution of conformist transmission, which suggests that the assumption of only two traits in many models has been conservative. We close by discussing how (1) spatial variability represents only one way of introducing the low-level, nonadaptive phenotypic trait variation that so favors conformist transmission, the other obvious way being learning errors, and (2) our findings apply to the evolution of conformist transmission in social interactions. Throughout we emphasize how our models generate empirical predictions suitable for laboratory testing.     

Can indirect selection and genetic context contribute to trait diversification? A transition‐probability study of blossom‐colour evolution in two genera

Darwin recognized that biological diversity has accumulated as a result of both adaptive and nonadaptive processes. Very few studies, however, have addressed explicitly the contribution of nonadaptive processes to evolutionary diversification, and no general procedures have been established for distinguishing between adaptive and nonadaptive processes as sources of trait diversity. I use the diversification of flower colour as a model system for attempting to identify adaptive and nonadaptive causes of trait diversification. It is widely accepted that variation in flower colour reflects direct, adaptive response to divergent selective pressures generated by different pollinators. However, diversification of flower colour may also result from the effects of nonadaptive, pleiotropic relationships with vegetative traits. Floral pigments that have pleiotropic relationships to vegetative pigments may evolve and diversify in at least two nonadaptive ways. (1) Indirect response to selection on the pleiotropically related nonfloral traits may occur (indirect selection). (2) Divergent evolution in response to parallel selective pressures (e.g. selection by pollinators for visually obvious flowers) may occur because populations are at different genetic starting points, and each population follows its own genetic `line of least resistance.' A survey of literature suggests that pleiotropic relationships between flower colour and vegetative traits are common. Phylogenetically informed analyses of comparative data from Dalechampia (Euphorbiaceae) and Acer (Aceraceae), based on trait‐transition probabilities and maximum likelihood, indicated that floral and vegetative pigments are probably pleiotropically related in these genera, and this relationship better explains the diversification of floral colour than does direct selection by pollinators. In Dalechampia pink/purple floral bract colour may have originated by indirect response to selection on stem and leaf pigments. In Acer selection by pollinators for visually obvious flowers may to have led to the evolution of red or purple flowers in lineages synthesizing and deploying red anthocyanins in leaves, and pale‐green or yellow flowers in species not deploying red anthocyanins in vegetative structures. This study illustrates the broader potential of indirect selection and parallel selection on different genetic starting points to contribute to biological diversity, and the value of testing directly for the operation of these nonadaptive diversifying processes.     

Bipedalism and human birth: The obstetrical dilemma revisited

…adaptation to bipedal locomotion decreased the size of the bony birth-canal at the same time that the exigencies of tool use selected for larger brains. This obstetrical dilemma was solved by delivery of the fetus at a much earlier stage of development. (Washburn¹) …there can be no doubt that many of the obstetrical problems of Mrs. H. Sapiens are due to the combination of a narrower pelvis and a bigger head in the species. (Krogman²)     

The relevance of brain evolution for the biomedical sciences

Most biomedical neuroscientists realize the importance of the study of brain evolution to help them understand the differences and similarities between their animal model of choice and the human brains in which they are ultimately interested. Many think of evolution as a linear process, going from simpler brains, as those of rats, to more complex ones, as those of humans. However, in reality, every extant species' brain has undergone as long a period of evolution as has the human brain, and each brain has its own species-specific adaptations. By understanding the variety of existing brain types, we can more accurately reconstruct the brains of common ancestors, and understand which brain traits (of humans as well as other species) are derived and which are ancestral. This understanding also allows us to identify convergently evolved traits, which are crucial in formulating hypotheses about structure-function relationships in the brain. A thorough understanding of the processes and patterns of brain evolution is essential to generalizing findings from 'model species' to humans, which is the backbone of modern biomedical science.     

How scientists perceive the evolutionary origin of human traits: Results of a survey study

Various hypotheses have been proposed for why the traits distinguishing humans from other primates originally evolved, and any given trait may have been explained both as an adaptation to different environments and as a result of demands from social organization or sexual selection. To find out how popular the different explanations are among scientists, we carried out an online survey among authors of recent scientific papers in journals covering relevant fields of science (paleoanthropology, paleontology, ecology, evolution, human biology). Some of the hypotheses were clearly more popular among the 1,266 respondents than others, but none was universally accepted or rejected. Even the most popular of the hypotheses were assessed “very likely” by <50% of the respondents, but many traits had 1–3 hypotheses that were found at least moderately likely by >70% of the respondents. An ordination of the hypotheses identified two strong gradients. Along one gradient, the hypotheses were sorted by their popularity, measured by the average credibility score given by the respondents. The second gradient separated all hypotheses postulating adaptation to swimming or diving into their own group. The average credibility scores given for different subgroups of the hypotheses were not related to respondent's age or number of publications authored. However, (paleo)anthropologists were more critical of all hypotheses, and much more critical of the water‐related ones, than were respondents representing other fields of expertise. Although most respondents did not find the water‐related hypotheses likely, only a small minority found them unscientific. The most popular hypotheses were based on inherent drivers; that is, they assumed the evolution of a trait to have been triggered by the prior emergence of another human‐specific behavioral or morphological trait, but opinions differed as to which of the traits came first.     

Functional aspects of pelvic morphology in simian Primates

In functional analyses of the Primate pelvis only selective forces resulting from locomotory functions have traditionally been taken into account, therefore neglecting possible selective forces resulting from obstetrical functions. This paper analyzes the nature, degree, and action of the selective forces acting on the pelvis of simian Primates which result from maternal-fetal size relationships and their interaction with selective forces resulting from locomotory functions. Based on the analysis of these factors in living Primates, an estimate of their degree and interaction in Australopithecus africanus is given to further elucidate the problem of the evolution of hominid bipedalism.     

Functional morphology of the human chin

The protruding chin is an attribute that defines modern Homo sapiens to the exclusion of all other primates, including fossil hominids. The functional significance of the chin has been contemplated for most of the 20th century, but as yet no compelling functional argument for its evolution has withstood careful scrutiny. Consequently, the human chin is often cited as an example of a nonadaptive trait. Past attempts to explain the chin in a functional or mechanical context have failed, largely as a result of an incomplete understanding of in vivo masticatory biomechanics. When the morphology of the chin is considered in light of experimental data on mastication, its evolution can be interpreted as a consequence of recent changes in mandibular proportions that have altered the relative importance of different masticatory stresses. Hypotheses proposing that chin morphology is the result of sexual selection or spatial constraints may be untestable. As with arguments that posit no functional role for the chin, the credibility of these hypotheses has depended, to a large degree, on the refutation of previous biomechanical explanations.     

Phylogeny and evolution of exaggerated traits among the Tingidae (Heteroptera, Cimicomorpha)

The Tingidae (Heteroptera) are characterized in part by their lace‐like structures. Some of the traits they exhibit, mostly on the hemelytra and the pronotum, can be considered as exaggerated. One may ask, are these traits hypertelic (nonadaptive) or do they represent an adaptation? Such a question is discussed with the support of a phylogenetic analysis of 55 taxa and on the basis of 85 characters. Six equiparsimonious trees are obtained by a first analysis. Three main groups are defined, but Tinginae appears paraphyletic, while Cantacaderinae, monophyletic, is included in Tinginae. Nevertheless, the relationships between the studied taxa show that there is a global tendency for pronotal and hemelytral traits to evolve from simple to exaggerated. Such evolution occurs in three clades independently. Thus, it is suggested that such traits could have an adaptive function, as also suggested for the pronotal expansions occurring on Membracidae (Auchenorrhyncha).     

Nonadaptive female pursuit of extrapair copulations can evolve through hitchhiking

Mounting evidence has indicated that engaging in extrapair copulations (EPCs) might be maladaptive or detrimental to females. It is unclear why such nonadaptive female behavior evolves. In this study, we test two hypotheses about the evolution of female EPC behavior using population genetic models. First, we find that both male preference for allocating extra effort to seek EPCs and female pursuit behavior without costs can be maintained and remain polymorphic in a population via frequency‐dependent selection. However, both behaviors cannot evolve when females with pursuit behavior suffer from a decline in male parental care. Second, we present another novel way in which female pursuit behavior can evolve; indirect selection can act on this behavior through a ratchet‐like mechanism involving oscillating linkage disequilibria between the target EPC pursuit locus and two other loci determining male mate choice and a female sexual signal. Although the overall positive force of such indirect selection is relatively weak, our results suggest that it may still play a role in promoting the evolution of female EPC behavior when this behavior is nonadaptive (i.e., it is neutral) or only somewhat maladaptive (e.g., males only occasionally lower parental care when their mates pursue EPCs).     

Evolution of self-organized systems

In this paper I ask questions about the evolution of self-organized activity cycles that are found in some ant colonies. I use a computer model that generates periodic activity patterns in interacting subunits and explore the parameters of this model using a genetic algorithm in which selecting on one aspect of the system produces the distinctive self-organized pattern. The general point that I explore, using the example of activity cycles, is that the observation of a self-organized pattern does not mean that the pattern is an adaptation. Self-organized patterns can represent nonadaptive correlated responses to selection, exaptations or even selectively disadvantageous traits. Evolution of self-organized patterns requires genetic feedback between the self-organized output and the subunits that produce the pattern. Without this necessary feedback, a self-organized system does not evolve.     

The concept of correlated progression as the basis of a model for the evolutionary origin of major new taxa

Understanding the evolutionary processes responsible for the long treks through morphospace associated with the origin of new higher taxa is hampered by the lack of a realistic and usable model that accounts for long-term phenotypic evolvability. The systems-related concept of correlated progression, in which all the traits are functionally linked and so constrained to evolve by small increments at a time in parallel with each other, provides the basis for such a model. Implications for the process of evolution at high taxonomic level are that: the evolving traits must be considered together as a system, and the exact sequence of incremental changes in characters is indeterminable; there are no identifiable key innovations; selection acts on the phenotype as a whole rather than on individual traits; and the selection force is therefore multidimensional. Application of the model to the pattern of evolution of traits and trait states as revealed by the fossil record of the stem groups of such taxa as mammals, turtles and tetrapods generates realistic testable hypotheses about how such groups evolved.     

动物生活史进化理论研究进展

综述了生活史性状、生活史对策、权衡、适合度及进化种群统计学等动物生活史进化领域的进展。权衡是生活史性状之间相互联系的纽带,分为生理权衡与进化权衡。适合度是相对的,与个体所处的特定环境条件有关,性状进化与适合度之间关系紧密。适合度是生活史进化理论研究的焦点。探讨动物生活史对策的理论很多,影响最大的是MacArthur和Wilson提出的r对策及K对策理论。随年龄的增长,动物存活率及繁殖率逐步下降的过程,称为衰老;解释衰老的进化理论主要有突变-选择平衡假设和多效对抗假设。进化种群统计学将种群统计学应用于生活史进化研究,为探讨表型适合度的进化提供了有效的手段。将进化种群统计学、数量遗传学及特定种系效应理论进行整合,建立完整的动物生活史进化综合理论体系,是当代此领域的最大挑战。     

Cumulative cultural dynamics and the coevolution of cultural innovation and transmission: an ESS model for panmictic and structured populations

When individuals in a population can acquire traits through learning, each individual may express a certain number of distinct cultural traits. These traits may have been either invented by the individual himself or acquired from others in the population. Here, we develop a game theoretic model for the accumulation of cultural traits through individual and social learning. We explore how the rates of innovation, decay, and transmission of cultural traits affect the evolutionary stable (ES) levels of individual and social learning and the number of cultural traits expressed by an individual when cultural dynamics are at a steady‐state. We explore the evolution of these phenotypes in both panmictic and structured population settings. Our results suggest that in panmictic populations, the ES level of learning and number of traits tend to be independent of the social transmission rate of cultural traits and is mainly affected by the innovation and decay rates. By contrast, in structured populations, where interactions occur between relatives, the ES level of learning and the number of traits per individual can be increased (relative to the panmictic case) and may then markedly depend on the transmission rate of cultural traits. This suggests that kin selection may be one additional solution to Rogers's paradox of nonadaptive culture.     

The evolution of gender-biased nectar production in hermaphroditic plants

The evolution of secondary sexual floral traits may be driven by selection through male or female reproductive success. Even so, the gender-biased function of a floral trait is often unapparent because secondary sexual traits and primary sexual organs of both genders co-occur within most bisexual flowers. Within dichogamous plants, however, secondary sexual traits may be unambiguously expressed in association with the primary sexual organs of one gender, making these species uniquely suited to studies of natural and sexual selection on floral traits. The objectives of this article are to summarize patterns of gender-biased nectar production and to critically explore theories relevant to its evolution. We list 41 species with gender-biased nectar production and provide two sets of adaptive hypotheses for the trait: sexual selection hypotheses and inbreeding avoidance hypotheses. We formulate these hypotheses using sexual selection theory in plants and the literature that relates pollinator foraging to plant inbreeding. We also consider explanations based on resource trade-offs, enemies, and genetic correlations. Support for the sexual selection and inbreeding avoidance hypotheses is provided by only a few well-studied species. We outline a series of experiments that should facilitate sorting among hypotheses. Plants with gender-biased nectar production are likely to provide unique insights into the roles of natural and sexual selection in the evolution of floral traits.