The Anthropology of the Fetus

Biology, Culture, and Society

Sallie Han, Tracy K. Betsinger, Amy B. Scott, Sallie Han, Tracy K. Betsinger, Amy B. Scott

• Publisher: Berghahn Books
• Year: 2017
• ISBN:
  9781785336928
• Edition: 1
• Topic: Medicine
• Subtopic: Gynecology, Obstetrics & Midwifery

As a biological, cultural, and social entity, the human fetus is a multifaceted subject which calls for equally diverse perspectives to fully understand. Anthropology of the Fetus seeks to achieve this by bringing together specialists in biological anthropology, archaeology, and cultural anthropology. Contributors draw on research in prehistoric, historic, and contemporary sites in Europe, Asia, North Africa, and North America to explore the biological and cultural phenomenon of the fetus, raising methodological and theoretical concerns with the ultimate goal of developing a holistic anthropology of the fetus.

Part I

THE FETUS IN BIOSOCIAL PERSPECTIVE

Chapter 1

THE BORDERLESS FETUS

TEMPORAL COMPLEXITY OF THE LIVED FETAL EXPERIENCE

Julienne Rutherford

The completely self-contained “individual” is a myth that needs to be replaced with a more flexible description.
(Margulis and Sagan 2002: 19)

The idea that the experience and environment of pregnancy constitute an event that produces a singular individual called the “fetus” presumes fetus as discrete entity: a fetus has a distinct body, a specific temporality (i.e., bounded by gestation), and a distinct genetic identity. In essence, something fundamental and bounded must be assumed about the identity of the individual. However, in this chapter I argue that a fetus is not an easily definable entity with clear boundaries. Certainly, a fetus can largely be defined by its existence situated within a specific time and place, but these tangible attributes obscure the spatiotemporal complexity of the fetal experience. This is not merely a semantic or conceptual puzzle but a biological reality, whose borders extend past the flesh and bone of an individual. This borderlessness is in large part due to the lived experience within the womb and the role of the placenta as the interlocutor between “mother” and “fetus”—genetically and somatically overlapping yet distinct entities existing simultaneously in overlapping yet distinct ecologies, in different life history phases.

To critique the concept of the fetus as a distinct biological individual, a brief discussion of the meaning of “individual” is warranted. There are multiple philosophical approaches to this discussion (and indeed entire literatures that are beyond the scope of this chapter, e.g., the sociolegal implications of fetal “personhood”). However, my focus is on biological concepts of individuality, given my broader focus herein on the biological experience of the fetus. This discussion is not exhaustive and is mammal-centric, but it is provided as an organizing starting point for the argument that follows. The biological concept of the individual is labile across varying, somewhat arbitrary, levels of organization (e.g., genetic distinction, physical separation from “others,” etc.) (Pepper and Heron 2008: 623, table 1; Wilson and Barker 2014). The conventional concept is that of a single organismal entity that is both genetically and physically distinct from others (e.g., one monkey) (Benson 1989). This entity can reproduce itself either alone via cloning or budding, or through sexual reproduction. The entity interacts biologically and socially with other individuals and with(in) an environment but has a distinct and isolated three-dimensional form that is spatiotemporally limited. This is an organism-centered view of biological identity (cf. Gould 1980: 129) that allows for a hierarchical framework as follows (Wilson and Barker 2014):

(1) An organism (e.g., a monkey)

(2) A part of an organism (e.g., a placenta)

(3) Groups made of organisms (e.g., a family, a troop)

Given this simple framework, what is the fetus? It seems to meet the definition of an organism, but it also resides within and is physically attached to another organism, its mother. As is the case for most vertebrates, the fetus is genetically similar and dissimilar to its mother, owing half of its DNA to its father. Further, the residence the fetus inhabits is shaped by maternal biological processes and events that in turn are shaped both in the moment and through the life course by socioeconomic and psychosocial inputs (Rutherford 2009; fig. 1.1). Thus, the conceptual borders that frame the definition of an “individual” are potentially hampering our view of what it means to be a fetus in a biological sense.

To develop the concept of a biologically borderless fetus connected to multiple individuals and life history stages, I use three interrelated frames: (1) genetic complexity, or how genetic inheritance and epigenetic modifications link us to past and future generations; (2) experimental connectivity, or how the historic experiences of our mothers shape who we are as fetuses and adults; and (3) placental synchronicity, or how the placenta is a part of not only our fetal bodies but also our preconception histories and our adult futures.

FIGURE 1.1. Spatiotemporal borderlessness of fetal experience.

Frame 1: Genetic Complexity

Who we are is shaped in some part by our genetic composition. I liken this to a musical composition (for a literal interpretation of genes as music, see Søegaard and Gahrn 2009), in which the notes on the page are intended to be played but are subject to transient circumstances that change how they are played: the timing, the duration, the omission, the improvisational noodling (Shank and Simon 2000). That composition is written most immediately by two parents, but of course their contributions are shaped by the genetic composition of their two parents, their four grandparents, their eight great-grandparents, and so on. We have incorporated basic knowledge of inheritance into our understanding of life to the extent that we don’t always grasp the weight, enormity, and complexity of its importance. In the sense that we are all individual genetic melting pots, the borders between individuals and bodies dissolve in meaningful ways. We contain strands of DNA that have persisted for millennia through our immediate families and tribes, as well as our species and genera and those other families and orders and classes and phyla and kingdoms. This has great bearing on our conceptualization of the biological fetus.

One of the main reasons this connection is so important to understand is because the genome is mutable within the life course in ways we are only now beginning to appreciate. Epigenetics is the phenomenon of mechanisms acting beyond the genes (Waddington 1942). Whereas the DNA sequence inherited at conception (“genome”) remains fixed across the life cycle, the “epigenome” comprises molecular processes that determine how genes are expressed in specific environmental contexts and which can be permanently modified by early life environmental experience. DNA is a tightly folded series of nucleotide sequences (“genes”) that form the chromosomes. To initiate gene expression within the cell nucleus, a specific sequence of nucleotides must be briefly unwound. Gene expression can be silenced by applying chemical locks that keep that sequence from being unwound. One prominent epigenetic mechanism involves the addition of methyl groups to regions of DNA that promote gene expression (Berger 2007). The addition of these groups to these regions (i.e., “hypermethylation”) locks down that sequence and, in effect, silences that gene. The formation of eggs and sperm as well as early embryogenesis are when most existing locks are erased and, in a sense, developmental trajectories reprogrammed. What is critical to understand is that this reprogramming is subject to experiences like maternal nutrition (Lillycrop et al. 2005), rearing behavior (Weaver et al. 2004), stress (Murphy and Hollingsworth 2013), and even larger societal pressures such as racism and the experience of discrimination (Sullivan 2013) and war (Rodney and Mulligan 2014)—essentially, the lived contemporaneous and historical experience of the mother that is itself a product of complex environmental interconnectivity.

This interconnectivity may span multiple generations. Several studies in humans and animal models demonstrate maternal and grandmaternal effects on offspring growth that are not explained by genetics alone. In humans, mothers who experienced famine conditions when they themselves were fetuses gave birth to small-for-gestational-age babies, with placental size varying as a function of the time of famine exposure (Lumey 1998). Further, the female offspring later gave birth to small babies, independent of adult maternal weight (Lumey 1992). Similar patterns have been demonstrated in nonhuman primates (Price and Coe 2000; Price et al. 1999) and rodents (Drake et al. 2005; Hoet and Hanson 1999). Evidence for the transmission of environmentally triggered epigenetic changes to offspring comes from a variety of animal models, for instance, showing that maternal protein restriction in a pregnant mouse predicts blood sugar in her great-grandoffspring (Benyshek et al. 2006). Similarly, studies have shown that exposing several generations of mice to maternal undernutrition yields decreased birth weights, which are restored to control range only after three consecutive generations of normal diet (Stewart et al. 1980). Epigenetic modifications in response to varying developmental environments likely underpin the large disparities in health that have come to define the lived experiences of many people, how inequality becomes embodied as biology (Gravlee 2009; Thayer and Kuzawa 2011.)

A fetus possesses DNA sequences that overall are distinct from but born of its mother and father. But this genetic code and the developmental and regulatory processes it shapes are forged in an ecological setting that is a function of experiences and processes that both precede the fertilization of an egg and extend beyond gestation, a phenomenon I explore below.

Frame 2: Experiential Connectivity

This understanding of genetic complexity—an alterable, flexible genetic code subject to mechanisms that respond to lived experience—is key to the frame of experiential connectivity. The fetus develops in the context of a complex gestational ecology that is informed by proximate maternal physiology, to be sure, but we must recognize that the boundaries of those “merely biological” processes expand outward in time and space to encompass an almost limitless range of genetic, epigenetic, political economic, dietary, familial, and additional factors occurring not only during that pregnancy but over the course of that woman’s life (Rutherford 2009).

In light of this temporally and spatially interconnected developmental context, the developmental origins of health and disease (DOHaD, aka the Barker hypothesis, fetal programming, developmental programming, developmental origins) paradigm has emerged to conceptualize links between early life characteristics—features such as maternal health during pregnancy, gestational age at birth, birth weight and size, number and sex of in utero siblings, early postnatal and juvenile growth and experience—and adult health and function. Robust findings across human populations and nonhuman animal species including primates indicate that we carry with us our fetal experience. Low birth weight, which is viewed as a reflection of some kind of intrauterine restriction or perturbation, has been linked to adult cardiovascular parameters (Adair et al. 2001; Barker 1995), metabolic syndrome (Armitage et al. 2004), inflammatory response (McDade et al. 2014), mental illness (Abel et al. 2010), and other personally and societally detrimental health outcomes, including reproductive function in females. In a profound biological sense, we do not leave behind our fetal identities even as we mature into adulthood, and reaching back into the past, our fetal identities are shaped by factors that precede our conception and even our mother’s conception.

My work on the early life factors that shape reproductive function in the common marmoset monkey illustrates this point. This species of marmoset monkey, like the other marmosets and tamarins, produces litters of variable size, typically observed as twins in the wild but ranging up to quadruplets and even quintuplets in captivity. Recent evidence suggests that triplet pregnancies occur across various marmoset and tamarin species in the wild as well (Bales et al. 2001; Dixson et al. 1992; Savage et al. 2009). Twins and triplets equally contribute to nearly 98 percent of all births in the marmoset colony at the Southwest National Primate Research Center, where my research team’s work is conducted. Our previous research has shown that triplet fetuses experience a nutrient- and growth-restricted environment relative to that experienced by twin fetuses, with increased perinatal mortality, lower birth weight, and accelerated postnatal growth (reviewed in Rutherford 2012). Low birth weight triplets are more likely than low birth weight twins to grow into exceptionally large adults (Tardif and Bales 2004), a phenotype seen in many humans who have experienced intrauterine nutrient restriction. This is consistent with the concept of “mismatch” in which the prenatal mechanisms that allow a fetus to adjust its growth to survive in restricted intrauterine environments are offset by differential developments of organ systems that are ill-prepared for postnatal environments of relative plenty (Godfrey et al. 2007). All of these outcomes have important implications for adult health.

Because of the importance of maternal ecology and history in shaping the developmental experience of fetuses, we asked whether adult reproductive function differs between adult twin and triplet marmoset females. Life history theory suggests there are tradeoffs between different biological functions and different life history phases. By extension, an investment in merely reaching thresholds of growth and development in the face of an impoverished intrauterine environment may mean that not all body systems develop optimally, particularly if they are not essential for survival. This could play out as maximal investment in the development of the brain, which is central to global functioning, with reduced investment in the nonessential-for-survival reproductive system. Thus, greater detriments experienced during fetal life may well affect adult reproductive functioning. Links between reduced birth weight and impaired adult reproductive function have been observed in many animals, including primates such as macaques (Price and Coe 2000) and humans (Lumey 1992, 1998).

The range of litter size in the marmoset monkey offers a type of “natural experiment” in variable intrauterine environments and long-term consequences for reproduction. Our team has taken advantage of this experiment to demonstrate startling variation in adult reproductive function as a result of developmental experiences (Rutherford et al. 2014). Extensive demographic records of the marmoset colony allow us to determine that twins and triplets in fact produce roughly the same number of fetuses, averaging around 9 spread over about 3.5 litters. However, adult triplet females lose those fetuses to spontaneous abortion and stillbirth at a much higher rate, nearly three times as great, regardless of current adult characteristics such as weight. As mentioned, because triplets tend to be born at lower birth weights, this disparity could be a residual effect of low birth weight. However, when matched to twins in terms of birth weight, triplet females still are losing a significantly larger proportion of fetuses as adult. This suggests that important developmental differences exist depending on the number of fetuses sharing intrauterine resources. It also means that growth does not equal size: the fetal body itself is shaped by complex temporal and developmental processes that do not always manifest in low birth weights (Jansson and Powell 2007; Sibley et al. 2005).

Female marmoset fetuses experience another burden in utero. Marmosets are not monozygotic (produced from a single ovum), so mixed-sex litters are common. Across all females, regardless of litter size, exposure to a brother in utero led to a threefold increase in fetal loss when they were adults. This “brother effect” is possibly due to the production of testicular androgens that masculinize the female reproductive axis, although the mechanisms of this process are currently not well understood. What is clear is that the presence of a brother in utero does play a role in the much higher fetal loss rate experienced by triplet females, but even when triplets from all female litters are compared to twins from all female litters, triplets still suffer greater loss as adults, suggesting that the complex intrauterine environment experienced by triplets reflects baseline disruption that is further exacerbated by exposure to...

Table of contents

• Cover
• Title Page
• Copyright Page
• Dedication
• Contents
• List of Illustrations
• Acknowledgments
• Foreword. How/Shall We Consider the Fetus?
• Introduction. Conceiving the Anthropology of the Fetus
• Part I: The Fetus in Biosocial Perspective
• Part II: Finding Fetuses in the Past: Archaeology and Bioarchaeology
• Part III: The Once and Future Fetus: Sociocultural Anthropology
• Conclusion
• Glossary
• Index