evolution

Physiological and Evolutionary Mechanisms of Fertility at High Altitude: Part 2

Birth weights, Stillbirth Rates, and Infant Mortality

Exposure to hypoxic environments may increase the stress on an already vulnerable growing fetus, thus result in a higher frequency of low birth weight, higher stillbirths, and increased infant mortality among high altitude populations. Several scholars have reported reduced birth weight with increasing altitude due to inadequate maternal oxygenation later in pregnancy (Yip, 1987; Haas et al., 1977; Ballew and Haas, 1986; Jensen and Moore, 1997; Khalid et al., 1997). For pregnant women, oxygen saturation and hemoglobin concentration naturally decrease towards term, resulting in a fall in arterial oxygen at the end of pregnancy. If a woman is at high altitude, she has even less access to oxygen which may explain the reduction in birth weight at high altitudes (Hartinger et al., 2006).

Hartinger and colleagues (2006) compared birth weights of 84,173 neonates between 1995 and 2002 from the cities of Lima (150 masl), Huancayo (3280 masl), Cusco (3400 masl), and Juliaca (3800 masl). The authors found that birth weight is lower at high altitude, but there is no linear relation between altitude of residence and birth weight (Hartinger et al., 2006). In fact, in Juliaca (3800 m) where the population has resided the longest, birth weight was higher than that of Huancayo (3280 m) where indigenous populations have resided the shortest. In Cusco (3400 m), where there is increased admixture among Spanish and indigenous populations, birth weight was also lower compared to Juliaca (Hartinger et al., 2006). The data suggests that women from families who had lived at high altitudes for at least 3 generations maintained their oxygenation better during pregnancy (McAuliffe, 2001), allowing for a higher birth weight and suggesting that adaptation occurs when groups are exposed to a hypoxic environment over generations (McAuliffe, 2001).

Several studies have confirmed an association between high altitude and a higher stillbirth rate (Gonzales et al., 2007; INEI, 2001) due to an effect of low barometric pressure and colder temperatures common in these hypoxic environments (Gonzales, 2007). For example, populations in the Sarata district of southern Peru almost 20 percent of children do not survive beyond age five (Collins, 1983). Local health personnel and native healers state that the leading cause of infant mortality is respiratory failure, possibly related to the hypoxic environment (Collins, 1983). In fact, respiratory symptoms are reportedly responsible for 58-68 percent of deaths among children under one year of age, and for 49-55 percent of deaths among children aged one to five (Collins, 1983).

To offset the effects of high altitudes, indigenous Peruvian mothers often tightly swaddle and enclose their infants in a set of clothes and blankets, referred to as a manta pouch. The manta pouch modifies the internal microenvironment so that, compared to the ambient environment, the temperature is higher and more stable, the humidity is higher, the partial pressure of oxygen is lower, and stimulation levels are reduced. It appears to be a solution the lower the infant mortality rate among indigenous women (Tronick et al., 1994).

Gonzales and colleagues (2007) compared stillbirth rates from a sample of 22,662 births between 2005 and 2006 for the cities of Lima (150 masl), Huancayo (3280 masl), Cuzco (3430 masl), and Puno (3850 masl), and reported that stillbirth rates were higher at high altitude (>3000m) compared with low altitude (Gonzales et al., 2007). Yet, inhabitants from the South Andes (i.e. Cusco, Puno) actually have lower stillbirth rates compared with the central Andes (Huancayo) (Gonzales et al., 2007). Similar to Passano (1983), Gonzales and colleagues attribute this discrepancy with a vague description of an “ancestry effect,” in which populations with longer multigenerational residence in the southern Andes population may be linked to lower still birth rates (Gonzales et al., 2007).

To summarize, there appears to be no association between an increase in fetal mortality with increasing elevation. High altitudes pose several environmental stressors (e.g. low oxygen and cold temperatures) which increase infant mortality; to counteract these stressors, Peruvian mothers tightly wrap and swaddle their newborns in mantas, creating a protective microenvironment. Interestingly, the rates of perinatal and neonatal mortality are, however, lower in populations that have resided at high altitude for longer; populations inhabiting the southern Andes have a longer antiquity at high altitude and lower rates of fetal and neonatal deaths than those in the central Andes with a shorter residence at high altitude.

Post-Partum Behaviors

Female physiology after birth may contribute to lower fertility levels, but most research has indicated that post-partum behaviors account for a decrease in reproductive rates. The National Institute of Statistics and Informatics of Peru documented longer durations of exclusive breastfeeding at high-altitudes than at sea level as revealed by an increased prevalence of lactation amenorrhea (absence of menstruation)(INEI, 2001). Yet, Gonzales (2007) noted that fertility rates among high altitude populations in Peru are higher compared to those at sea level despite the prevalence of lactation amenorrhea and prevalence of >2 years sexual abstinence after parturition.

Couples living in the Sarata district of Peru take an active role in preventing and regulating births family sizes after reaching the desired number of children size. Collins (1983) reported that women sought herbal specialists who provided herbs, fruits, and seeds thought to induce miscarriages if taken within a month or two of conception. Infanticide is also a common practice, especially if the infant was in some way abnormal, because the harshness of the environment and lack of health care services made the burden of raiding an abnormal or weak child too costly for many families. Other methods approved by the local Catholic nuns included abstinence and the rhythm method. Also, seasonal migration is sometimes prescribed to young couples that were having children more rapidly, and Collins (1983) noted two accounts in which fathers-in-law recommending that their sons–in-law migrate seasonally in order to space births.

Similarly, Laurenson and colleagues (1985) noted that females living in Central Nepal (12,400 feet) experienced lower fertility frequencies than females living at 8500 feet. Though the females at high altitudes reported longer post-partum ammenorhea and breast-feeding periods, the pregnancy gap was due to the later age of marriage and controlled birth spacing (Laurenson, et al., 1985). Overall, it appears that both male and female parents actively seek solutions to control birth spacing in order to achieve desired number of offspring.

Onset of Menopause

Similar to the age of sexual maturation, high altitudes may contribute to an earlier or later onset of menopause. Studies have documented that the age at menopause occurs earlier at high altitude than at sea level (Gonzales, 1994) and therefore result in a shorter reproductive span for women living at altitude (Gonzales and Villena, 1996). Women living at Cerro de Pasco (4340 masl) experienced accelerated menopause compared to women in Lima (150 masl) due to high levels of serum follicle stimulating hormone (FSH) and accelerated oocyte loss observed in regularly menstruating women at high altitude (Gonzales and Gonez, 2000).

Studies have estimated medium age of menopause to be between 45.4 years and 46.1 years among rural Bolivian Aymara, (Crognier et al. 2002; Burch and Vitzthum, 2011). Among women living at high altitude in Nepal, menopause occurs between 45–50 years (Lang and Lang, 1971; Beall, 1983), an age range that is within the average onset of menopause worldwide. Vitzthum (2013) notes, however, that these ranges are similar to those of other populations that have poor living conditions and high mortality risks (e.g., India = 44.0 years; also see Wood, 1994). Like age at menarche, variation in age at menopause may be due to factors other than, or in addition to, hypoxia. Yet, there appears to be little, if any, demographic impact of perhaps a year less at the end of the reproductive life span of women (Vitzthum, 2013).

Evolutionary Mechanisms and Ethnicity/Ancestry Influences on Fertility

Evolutionary processes may have acted differently on the populations who originally migrated into high altitude environments and thus resulted in different patterns of adaptation. These results suggest that longevity of life at high altitude may be an important component of adaptation. For example, the reduced survival of Spanish children at high-altitudes suggests that the newcomers lacked an adaptation to the hypoxic environment (Gonzales, 2007). The indigenous Peruvian population—Aymara and Quechua—was later mixed with the Spaniards who colonized Peru during the 16th century. As a result, the Peruvian population has three important admixture groups: first, the Quechua or Aymara populations with long-term residence in highland zones particularly at the Southern Andes (Cuzco and Puno), and the second is admixture of Spanish with the indigenous Quechua and Aymara populations, and third, the Spanish who moved to high altitude relatively recently in the last four centuries (Rupert and Hochachka, 2001). This introduction and mixture of genes may have stopped or reversed the adaptive processes preformed during more than 10,000 years of life at high altitude. Natives with longer ancestry in high altitudes appear to have an unknown genetic component that make them better adaptive to their environments compared to individuals of Spanish descent.

Evolutionary processes may have acted differently on colonizing populations of the Andes verses those of the Himalayas, resulting in different pattern of adaptation (Beall, 2006). Compared to Andean residents, Tibetans with 20,000 years of antiquity at high altitude demonstrate less intrauterine growth retardation and elevated arterial oxygen content which increases uterus-placental oxygen delivery during pregnancy (Moore et al., 2004; Wiley, 1994). The ability to sufficient deliver oxygen to the fetus and the fetus’ ability to incorporate the oxygen into its system is necessary for the offspring’s survival (Moore et al., 2004; Wiley, 1994).

It appears that a phenotype of high saturation of oxygen may exist among populations with antiquity in high altitude environments. For example, Bealls’ (2006, 2007) research has supported the hypothesis that the higher oxygen saturation allele might be favored by natural selection among Tibetans, but not Andean peoples. To test the hypothesis that high oxygen saturation genotypes have higher Darwinian fitness, Beall (2006, 2007) gathered genealogical, oxygen saturation, and female fertility data from 905 households in 14 villages at 3800-4200 masl in rural areas of the Tibet Autonomous Region and found that infants who were homozygous and heterogygous for oxygen saturation gentoypes had higher likelihood of surviving infancy (Beall 2006, 2007, 2014). This suggests that high-altitude hypoxia acts as an agent of natural selection on the heritable quantitative trait of oxygen saturation via the mechanism of higher infant survival of Tibetan women with high oxygen saturation genotypes (Beall et al., 2004; Beall, 2006, 2007, 2014).

In sum, there are evolutionary forces selected for increased oxygen saturation among Tibetan populations with the greatest antiquity in the Himalayas. Though Andean samples lacked the allele associated with this mechanism, it is possible that similar adaptive forces have been acting on the indigenous populations of the Andes.

Discussion

Historic chroniclers found that indigenous Andean females maintained capacity to reproduce while Spanish colonists were reportedly unable to carry fetus to full term or experienced high infant mortality rates. Low oxygen environments may delay the onset of sexual maturation among Himalayan and Andean populations; however, menarcheal age is well within the range of variation worldwide. Whether or not socio-economic status impacts sexual maturity remains unclear. Overall, it appears to have no demographic consequence because marriage and sexual behaviors typical begin well after puberty between highland Himalaya and Andean populations. Studies documenting gamete formation and testosterone production have demonstrated that exposure to high altitudes negatively impact male reproductively abilities for a short period of time. Mechanisms of ovulation vary between highland and lowland females in both the Andes and Mongolia yet are well within the range of worldwide variation. At times, differential barometric pressures appear to impact female ovulation, but there appears to be no negative impact on female fertility. In fact, it appears that overall health and socioeconomic status may impact overall fertility among high altitude populations. Lower oxygen levels may be linked to lower birth rates among high altitude infants, yet there is no linear relation between altitude of residence and birth weight. In fact, better oxygenation during pregnancy appears to be an adaptation among women with greater ancestral antiquity in high altitudes. Low barometric pressure and cold temperatures are traits of high altitudes and are attributed to the high stillbirth and infant mortality rates. Infants born into populations with greater antiquity in the highlands, however, appear to be more likely to survive compared to infants born to recent immigrants to the highlands. Post-partum behaviors such as breast-feeding, abstinence, herb-inducing miscarriage, and rhythm method, indicate that females actively attempt to regulate reproduction and control birth spacing, thus actively attempt to control their fertility.Variation in age at menopause between highland and lowland populations may be due to hypoxic environments as well as poor living conditions and overall health. However, there appears to be little, if any, demographic impact on the earlier age of menopause among women in high altitudes.

The stressors associated with high-altitude environments impose severe, lifelong stress upon every resident regardless of age, sex, or individual characteristic. Populations living in high-altitude environments do not adapt behaviorally to create non-hypoxic microclimates, people must adapt biologically. In fact, genetic research is beginning to elucidate the how populations with the longest antiquity in high altitudes have certain genes that allow them to live, and thrive, in an otherwise physiological stressful environment.

Conclusion

High altitude environments appear to impact the reproductive physiology of males and females, yet individuals who have a longer ancestry at high altitude appear to have adapted to the low oxygen environments. While socioeconomic factors sometimes negatively impact fertility, it appears that high altitude ancestry appears to have a greater impact on reproductive success. Native populations with a long ancestry in high altitudes have fewer reproductive issues while those who have a mixed ancestry (e.g. Spanish verses Quechua or Aymara; Han Chinese verses Tibetans), are more likely to have issues with fertility. In sum, an examination of fertility in the Andes and Himalaya mountains illuminates complex relationship between proximate behaviors and dynamic evolutionary adaptations which together impact reproductive functioning in high altitude environments.

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Physiological and Evolutionary Mechanisms of Fertility at High Altitude: Part 1

High altitudes have the potential to negatively impact normal bodily functions of individuals who are both accustomed, or not properly acclimated, to such environments. Air deficient in oxygen, colder temperatures, greater exposure to solar radiation, and higher energetic costs of subsistence compared to that of lowland environments are potentially detrimental to physiological function. Similarly, high-stress environments with riskier living conditions may lead to economic disparities and locally specific cultural practices. Despite these limitations, human populations have lived, and thrived, in high altitudes environments for thousands of years. I investigate how theses environmental stressors impact reproductive functioning and fertility of indigenous populations living at high altitude, particularly in the Andes and Himalaya Mountains. In particular, I assess whether or not altitude-related stressors and reproductive behaviors contribute to lower fertility rates among high altitude populations. Through analysis of the physiological, behavioral, and genetic properties of males and females living at high attitude, I argue that fertility rates are under strong evolutionary control that offset altitude-induced sicknesses (hypobaric hypoxia) thus limiting variation in fecundity among high altitude populations.

History of the Study of Fertility at High Altitudes

Populations and small-scale societies have a long antiquity at high altitudes, yet much of our early knowledge of whether or not males and females had normal reproductive fitness comes from chronicles written by Europeans colonizing the Andes. Archaeological investigations in the Andes are numerous and are ongoing (Rademaker et al., 2014), yet are still in a very early stage in the Himalaya Mountains (Aldenderfer, 2011). Similarly, studies of the genetic components associated with high-altitude living are novel avenues of investigation among researchers working with populations in both the Andes and Himalayas (Beall, 2006, 2007). Given this incomplete picture, fertility studies conducted among populations living in other high altitudes (e.g. ovulation among Mongolian females) will also be presented when relevant. Because both the Andes and Himalaya Mountains are both extreme high altitude environments, I will explore research on reproductive fitness from both areas while recognizing that the entire picture elucidating the nature of fertility at high altitudes remains incomplete.

It is generally assumed that the human ancestral phenotype of oxygen transport system evolved mainly in environments with normal oxygen levels, or “normoxia” at sea level (Beall, 2006; Hochachka et al., 1998). Geological, vegetational, and archaeological analyses of hominin fossil sites in rift valleys formations in Ethiopia spanning approximately 3 million years indicate that hominid habitation sites were at an altitude of 500-600 meters above sea level (masl), well below an altitude thought to induce hypoxic stress (Bonnefille et al., 2004; Redfield et al., 2003; Quade et al., 2004). Thus, it is assumed that hominid evolution occurred under normoxia, and the corollary that high-altitude hypoxia is a physiological stress seems reasonable (Beall, 2006).

Laguna Cullicocha (4635 masl)

Laguna Cullicocha (4635 masl)

Altitude stress, medically known as hypobaric hypoxia, is cased by the fall in barometric pressure with increasing altitude, resulting in fewer oxygen molecules in a breath of air compared to sea level (Beall, 2006). Barometric pressure decreases with ascending altitude, decreasing oxygen availability in ambient air. Conditions are especially prevalent in the altiplano/puna, a treeless, tundra-like landscape higher than 4000 masl, with little fuel for campsites, and is an area that requires twice the sea-level caloric intake needed to maintain normal metabolic function (Marriot, 1996). Hypobaric hypoxia becomes progressively more severe with increasing altitude and stresses biological systems because a steady, uninterrupted supply of oxygen is required for metabolism in the mitochondria (Beall, 2006). Aside from supplemental oxygen or descent, there is no such strategy to avert the effects of environmental hypoxia (Gonzales, 2007; Julian, 2011). Though hypobaric hypoxia is the most pervasive physiologic challenge associated with high-altitude exposure, lower humidity, colder temperatures, increased solar radiation, and high energetic costs of subsistence that also accompany higher elevations may also threaten physiological well-being and reproductive behavior (Baker and Little, 1976).

Despite these stressors, human populations have occupied high altitudes for thousands of years. Archaeologists have uncovered ample evidence of human residency in high altitude environments as early as 20,000 years ago (Rademaker et al., 2014). The Tibetan Plateau of the Himalaya Mountains exhibits archaeological evidence of worked stone (Aldenderfer, 2011) and handprints and footprints (Quesang site) at 4200 masl (Zhang et al., 2002). Butchered animal bones, stone artifacts, and small-scale hearths dating from 14,600 to 7500 calendar years before the present (cal yr B.P.) at Jiangxigou 1 (~3200 masl); Heimahe 1 (~3200 masl) (Brantingham and Gao, 2006); at Xidatan 2 (~4300 masl) (Brantingham et al., 2013); and at Yeniugou (3800 masl) in the northeastern part of the plateau (Tang et al., 2013).

Tibetan Plateau (approx 4500 masl)

The earliest archaeological evidence of human occupation in the South American Andes dates to as early as 10,000 to 12,000 years BCE (Rademaker et al., 2014; Bonavia, 1991). The Pucuncho Basin in the southern Peruvian Andes contains the highest-altitude Pleistocene archaeological sites yet identified in the world (4355 masl) dating to 12,800-11,500 (Rademaker et al., 2014). Additional evidence of human occupation above 4000m of altitude with an antiquity of 10,000 years also has been found at the sites of Lauricocha, Huanuco (3850m) (Cardich, 1960) and Telarmachay, San Pedro de Cajas (4400m) in the Peruvian Andes (Bonavia, 1991).

Spanish chroniclers began to note the effect high altitude environments in the Andes had on living organisms during the 16th and 17th centuries early after colonization of the New World. Conquistadors such as Cieza de Leon (1553) described much about life among the Inca during the Spanish conquest and noted that the Inca had a surprisingly high fecundity rate. It was evident that Spaniards could produce offspring up to 3400 masl, yet infertility and stillbirths were frequent among Spaniards living in settlements around and above 4000 masl (Gonzales, 2007). Early chroniclers such as de la Vega and Cobo were of the opinion that the altitude effects on organisms were mainly attributable to the cold (de la Vega, 1609; Cobo, 1653). De la Calancha (1639) remarked in his chronicle that in Potosi (4300 m), in modern-day Bolivia, the natives had normal fertility and the offspring survived, whereas Spaniards encountered problems in having descendants. In fact, it was not until 53 years after then Spaniards settled the Andes did de la Calancha (1639) describe the birth and survival of the first child from two Spaniards in Potosi (4300 masl). Overall, chroniclers found that indigenous Andean females maintained capacity to reproduce while Spanish colonists were reportedly unable to carry fetus to full term or experienced high infant mortality rates.

Drawing by Guaman Poma de Ayala (1615/1616)

Given the discrepancy of fertility rates between newcomers to the Andes and the indigenous peoples, local biologists, biological anthropologists, and geneticists began to investigate the manner in which high altitude environments impact reproduction. Yet, many studies tend to produce contradicting results. The first fertility studies investigated the effects of altitude on fertility among sheep, cattle, cats, and rabbits, and demonstrated that short-term exposure to high altitude resulted in temporary infertility (Monge, 1942, Monge and Mori- Chávez, 1942; Monge et al., 1945).Studies in the late 20th century have shown that fertility is lower in the economically underdeveloped areas of the Andes than in the more prosperous Spanish-speaking parts (Collins, 1983). Studies documenting the fecundity rate (as calculated by the number of viable offspring per female) among Peruvian highlanders has found to be from one to two births less than that of lowland Peruvians of the same ethnic background. In fact, highland natives who move to low altitudes show markedly higher rates of fertility than their counterparts who remain in the highlands (Abelson, 1976). Conversely, studies have also noted that population fertility appears to be unaffected among natives to high altitude environments (Hoff, 1984). A retrospective hospital-based study performed on women of La Paz (3600 m), Bolivia shows that high altitude does not impair fertility (Suarez-Morales, 1967). In fact, the number of viable offspring born per female in the Andes has also been documented to be higher amongst high-altitude populations compared to those at sea level, suggesting that high altitude does not reduce fecundity in human populations (Gonzales, 2007). Additionally, scholars have noted that highlanders of both the Andes and Himalayas have distinctive morphological and physiological characteristics that seemed adaptive in the sense that they might offset hypoxia stress (Baker and Little, 1976; Monge, 1978). Given the complex and sometimes conflicting nature of the fertility data, considerations of the physiological mechanisms of reproduction as well as behavioral and genetic profiles will elucidate the nature of fertility at high altitudes.

Physiological and Behavioral Impacts on Fertility and Reproduction

At high altitude, the oxygen transport system must offset ambient hypoxia in order to maintain tissue oxygen levels to support maintenance, growth and development, and reproduction. Altitude-induced stress, hypoxia in particular, may act to affect the process of reproduction at several stages: formation of gametes and gametogenesis, the ovarian cycle and menstruation, birth weights, still birth rates, infant mortality, post-partum behaviors, and age of menopause.  Assessing how hypoxic stress impacts fertility alone is problematic because fertility is also affected by many cultural, social, and behavioral factors. Populations residing at high altitudes may have less developed health, social, and communication infrastructures than those residing at sea level. These reproductive categories will be explored while considering socioeconomic disparities and cultural practices impacting fertility. Over the next few weeks, I will address each of these reproductive systems beginning with development and formation of gametes and testosterone levels.

Development and Formation of Gametes and Testosterone Levels

Delay in the development of and abnormal formation of gametes may also impact fertility. In particular, research has documented whether or not male reproductive functions are negatively affected during and after high altitude sojourns. Early studies conducted on guinea pigs taken to Morochocha, Peru (4500m), observed degenerative alterations in the seminiferous tubules, which serve a crucial role in the production of male gametes (Guerra-Garcia, 1959).

Exposure to hypoxia and physical stress of high altitudes may induce reversible spermatogenic and/or Leydig cell dysfunction, a condition that decreases testosterone production (Saxena, 1995). Analysis of gamete production conducted on three subjects who trekked for 21-24 days between 5100-6700 masl revealed an increased rate of abnormal sperm shape (Abramsson et al., 1982), which would present an important problem if the subjects wanted children (Okumura et al., 2003). Additionally, scholars have observed that sperm counts had not recovered 3 months after subjects returned from the expedition. Yet, all subjects had normal gamete production and formation after 2 years (Okumura et al., 2003). Okumura and colleagues (2003) also observed an increase in abnormally shaped sperm 1 month after the subjects returned to sea level. Sperm shape had nearly recovered to the pre-expedition state after 3 months (Okumura et al, 2003).

Mount Everest (8848 masl)

In addition to hypoxia, physical stress while trekking and carrying heavy loads may also contribute to the initial decline in testosterone levels (Okumura et al., 2003). Endocrine tests conducted on the three subjects revealed slightly lower levels of testosterone in the blood 1 month after the expedition and decreased still further after 3 months. After 2 years, testosterone levels were normal. The subjects in the study also complained of erectile dysfunction after returning from the expedition, which may have been partly due to decreased testosterone (Okumura et al., 2003).

Semen analysis and recorded reproductive hormone levels taken from seven male mountaineers trekking through the Himalayas (approximately 5900 masl) found that physical exercise at high altitudes is associated with a testicular dysfunction leading to a reduced sperm concentration probably through an altered spermiation (Pelliccione et al., 2011). Interestingly, the physical exercise improved the male’s overall body composition, which increased testosterone levels after the expedition (Pelliccione et al., 2011).

In sum, studies have demonstrated short-term exposure to high altitudes negatively impact male gamete formation and testosterone production, ultimately affecting his ability to reproduce. It should be noted, however, that male gametes production and testosterone levels return to normal once he returns to sea level for several months to 1-2 years.

These are very high altitudes where people do not reside. Historically and in the archaeological record, however, there is evidence that people would take occasional sojourns to high mountain summits in the Andes. Spanish chronicler Cobo (1653) described how the Inka embarked on ritual pilgrimages (qhapaq huachas) to mountain summits were they would leave female and male children of exemplary physical perfection as immolate tribute to the Inka Empire and mountain gods. Freeze-dried bodies of these sacrificed children have been recovered from mountain summits up to 5200 masl in Chile, Argentina, and Peru (Reinhard and Ceruti, 2000). Physiologically, even brief sojourns to extreme altitudes has a minor impact on the reproductive system.

Ovarian Cycle and Menstruation

Ovulatory disorders are a major cause of infertility (Urman et al., 2006). While follicle phase ranges vary among women, a luteal phases lasting for less than 2 weeks is considered a “luteal defect” due to low levels of the hormone progesterone and an insufficient production of uterine lining, which inhibits a female’s reproductive abilities. Fecundability may be correlated to cycle length, which determines the number of opportunities for conception in a given time span (Wood and Weinstein, 1988). Because ovarian follicle growth is characterized by cell growth and rapid cell divisions, hypothetically, hypoxia may slow this process and thereby disrupt phase lengths (Wood and Weinstein, 1988).

Recent studies have suggested that short-term exposure to high-altitude hypobaric hypoxia may negatively impact the development and function of the corpus luteum. Parraguez and colleagues (2013) examined the corpus luteum among sheep living in high altitudes and found a significant decrease the growth and function of the corpus luteum, which resulted in decreased fertility (Parraguez et al., 2013). However, it is important to note that sheep used in the study were Creole ewes, a mixed breed developed from Churra and Manchega Spanish breeds brought to the Americas by Spanish colonists and therefore do not have a long ancestry in high altitude environments (Parraguez et al., 2013).

Among indigenous Aymara women on the altiplano (3800+ masl) of the Peruvian and Bolivia Andes, Vitzthum and colleagues (2000) reported a mean cycle length of 29.1 days (n = 612 cycles, 191 women). Cycle length among nomadic herders from the Mongolian high steppe (~1,500 masl) was 27.8 days, with the mean follicular-phase length averaging 14.7 days, and mean luteal-phase length 13.2 days (Jurado et al., 2009). According to Vitzthum (2009), neither the Aymara nor Mongolian cycle ranges were particularly low or high compared to cycle length of female populations worldwide. If hypoxia does slow follicle growth, the effect is insignificant (Vitzthum, 2013).

Differential hormone profiles, specifically time between the gonadotropin peak/release of luteinizing hormone (LH) and ovulation, between high and low altitude populations may indicate an ovulatory disorder. Escudero et al. (1996) compared samples from Lima (150 m) (N=10) and Cerro de Pasco (4340) (N=10), Peru. Females in Cerro de Pasco had smaller pre-ovulatory follicle diameters and lower estrogen production during the late follicle phase. Estradiol levels only increased 80% between Cerro de Pasco females compared to 137.3% among females in Lima. Additionally, the luteinizing hormone peaked earlier among women in Cerro de Pasco compared to women in Lima. Yet, both groups of females exhibited the same duration of the luteal phase and the same endometrium measurements between high and low altitudes (Escudero et al., 1996). Escudero and colleagues (1996) conclude that the differences in hormone profiles during menstrual cycle between high altitude and sea level samples are a result of low barometric pressure.

Conversely, Vitzthum and colleagues (2001a) compared ovulation rates between indigenous “middle-class” women in La Paz (3650 masl), Bolivia, and rural women living outside La Paz in El Alto (4150 masl), and reported that the rural participants had lower ovulation rates compared to the urban middle-class women, indicating that the difference in ovulation rates is not attributed to hypoxia because the two samples reside at similar altitudes (Vitzthum et al., 2001a, 2009). It is possible that overall health and socioeconomic status may impact overall fertility, yet the differences in ovulation lengths between the middle class and rural women may reflect normal variation (Vitzthum et al., 2001). The differences in ovulation may be correlated to socioeconomic status; ultimately, however, the high altitudes and sea level samples fall within the normal ranges of phase length and do not negatively impact reproduction.

Works cited in Parts 1 and 2 

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Abramsson, L.; Beckman, G.; Nordenson, I. (1982). Chromosomal aberrations and male infertility. J. Urology, 128, 52–53.

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Baker, P.T. and Little, M.A. (1976). Man in the Andes: A multidisciplinary study of high-altitude quechua: US/IBP Synthesis Series 1. Dowden, Hutchinson and Ross, Inc., Stroudsburg, PA.

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Beall, C.M. (2006). Andean, Tibetan, and Ethopian Patterns of Adaptaiton to High-Altitude Hypoxia. Integrative and Comparative Biology, 46, 18-24.

Beall, C.M. (1983). Ages at menopause and menarche in a high-altitude Himalayan population. Annual Human Biology, 10, 365-370.

Beall, C.M., Kijoung, S.; Elston, R.C.; Goldstein, M.C. (2004). Higher offspring survival among Tibetan women with high oxygen saturation genotypes residing at 4,000 m. Proceedings for the National Academy of Science, 101, 14300-14304.

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Brantingham, P.J.; Xing, G., Madsen, D.B.; Rhode, D.;  Perreault, C.; van der Woerd, J.; Olsen, J.W. (2013). Late occupation of the high-elevation Northern Tibetan Plateau based on cosmogenic, luminescence, and radiocarbon ages. Geoarchaeology 28, 413–431.

Brantingham, P.J. and Gao, X. (2006). Peopling of the northern Tibetan Plateau. World Archaeology, 38, 387–414.

Burch, J.C.; Vitzthum, V.J.; (2011). Project REPA: the timing of menopause in a population with high mortality risks. American Journal of Human Biology, 23, 254.

Cardich, A. (1960). Investigaciones prehistoricas en los Andes peruanos. In: Antiguo Peru: Espacio y Tiempo. Libreria Editorial Juan Mejia Baca, Lima, 89-118.

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Collins, J.L. (1983). Fertility Determinants in a High Andes Community. Population and Development Review, 9, 61-75.

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De La Calancha, A. (1639). Cronica Moralizadora de la Orden de San Augstin Imprenta Pedro Lacaballeria, Barcelona, Spain.

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This week in anthropology

Map of Native American tribes you have never seen before 

Mayan cities rediscovered in the Yucatan 

Subway in the sky, new cable car system to link La Paz with El Alto on the plateau 

Peruvian artisans win cash award for weaving in textile contest 

Lessons from the last time civilization collapsed 

“Consider this, if you would: a network of far-flung, powerful, high-tech civilizations closely tied by trade   and diplomatic embassies; an accelerating threat of climate change and its pressure on food production; a rising wave of displaced populations ready to sweep across and overwhelm developed nations. Sound familiar?”

Archaeologists uncover first mass grave from 14th century bubonic plague outbreak, Barcelona

 

What makes humans special? A graphical tour of  our evolutionary advantages starts with anatomy 

The problem when sexism sounds friendly (in academia) 

Are Neanderthals human? Scientist discuss whether or not Neanderthals belong with homo sapiens 

Pre-Columbian mycobacterial genomes reveal seals as a source of New World human tuberculosis

Irish fair skin can be traced back to the Middle East and India 

European man’s remains found in ancient Chinese tomb

Homo floresiensis: scientists clash over claims ‘hobbit man’ was modern human with Down’s syndrome

Meet The Generation Of Incredible Native American Women Fighting To Preserve Their Culture

World’s first 3D printed vertebra implanted in 12-year-old boy

Four Cases of Life-Threatening Plague Found in Colorado

 

 

 

 

 

This week in anthropology, bio anthropology, primatology, and bioarchaeology

The scourge of scurvy (vitamin C deficiency) and the demise of Europe’s first settlement in the Western Hemisphere

Mummy of Egypt’s “lost queen” Queen Hatshepsut found, osteological shows died of bone cancer around age 50 

Sharon DeWitte of University of South Carolina, using dental and skeletal evidence to look at populations before, during, and after Black Death swept Europe 

Mexican archaeologist excavate 1600 year old shaft tomb in State of Zacatecas, material evidence suggests the 28 individuals armed for battle in death

Neanderthal moms had it tougher than modern moms, Neanderthal and homo sapien infants had same cranial size at birth, and Neanderthal children grew at faster rates 

Getting to the root of enamel evolution: Connecting genes to hominin teeth shows evidence of natural selection 

Is ignorance bliss? The frustrations of being scientifically literate 

Byran college loosing 25% of faculty after “Adam and Eve” controversy 

Genes made us do it: the new pseudoscience of racial differences see also a great follow up Things to know when talking about race and genetics

Primates and patience: the evolutionary roots of self-control 

Chronicle of higher ed: struggling to find a project that excites you? follow these steps 

Function of human appendix, known use since lost?

Power and glory of the Maya queens, stele at Naachtun depicts fierce-looking, possible warrior, queen

Girl’s 12,000 year old skeleton found in underwater cave may shed light on Native American origins 

Should human remains be put on display? Archaeology and grave robbing 

Five ways twitter can be useful in academic contexts 

In Victorian ear, doctors prescribed beards to keep men healthy 

Restorers to bone up on skills for Kutná Hora ossuary makeover, Prague 

Bone to be wild, fleshing out a career devoted to skeletons and people, tribute to paleopathologist Dr. George Armelagos

Qatari people carry genetic trace of early migrants out of Africa  

Testing on Egyptian coffin’s wood reveals climate change may have caused empire’s fall 

Mountain Gorilla, Cross River Gorilla, and Sumatran Orangutan listed as some of the world’s most endangered animals 

Ancient faeces reveals origins of Puerto Rican natives 

Graphic of Wari woman’s royal tomb reveals burial fit for a queen, Peru 

Federal government jeopardizes Navajo’s family ties to home lands

Is your baby American enough Complicated relationship between genetics and nationality 

This week in anthropology, forensics, bioarchaeology, archaeology, and human evolution

Differences in core body temperature between men and women 

Lead in Rome’s water was 100 times higher than natural levels 

Study finds that Americans have more skepticism than confidence in scientific theories that are farther away from bodies in scope and time: global warming, the age of the Earth and evolution and the Bing Bang

After death, resurrection through decomposition and purification of the body 

Two 26th dynasty tombs unearthed near Minya, Egypt 

Humans may have dispersed out of Africa earlier than thought 

What is anthropology? 

Darwin’s tragic error: How Hitler and the Nazi’s destroyed evolution and propagated racism 

West Suffolk: Roman skeletons discovered by Anglian Water in Barnham, Bardwell, Pakenham and Rougham

A tomb of 49,000 year-old Neanderthal bones discovered in El Sidron, a remote, mountainous region of Northern Spain, leads to a compelling investigation to solve a double mystery: How did this group of Neanderthals die? (video) 

Scientists use CT scan to examine Inca mummy, the Ice Maiden, discovered in Argentina 

15 ways to tell if a science news story is hogwash 

Students in Oklahoma know less about evolution after taking biology 

Where Ancient Romans poisoned by lead?

Examining the Egyptian mummy, Tamut 

New support for Southern dispersal theory (out of Africa along South and Southeast Asia) 

The mind bending power of color, finally getting scientific notice? 

Suspected mass grave excavated in Serbia, believed to have remains of 250 Albanians from Kosovo War 

Creationists say government, Smithsonian is pushing “religion of naturalism” and “religion of evolution” on students 

Swedes open coffin of 850-year-old King Erik 

Everything from 4500-year-old site in California was excavated and then reburied

Using remote surveillance to monitor “uncontacted” Brazilian societies

Women undergoing foot surgery so they can wear designer shoes comfortably 

Stonehenge rock source identified 

Scientists discover little genetic variation among Neanderthals 

Education may insulate the brain against traumatic injury 

Ebola outbreak, crisis for primates and humans 

Durham academic finds 3,000 year old skeleton with clogged arteries 

 

This week in Anthropology, Forensics, Biological Anthropology, and Primatology

Shifting evolution into reverse promises cheaper, greener way to make new drugs

If humans used animal mating rituals

Peru has recovered over 8000 stolen cultural artifacts in the last seven years 

Spanish potsherds evidence of battle between Spanish and Native Americans on Great Plains 

Early Roman irrigation system uncovered in Britain 

10 oldest diseases like smallpox, cholera, and pneumonia 

Science compared every diet and the winner is no one 

UNESCO praises Peru’s work in combating illicit artifacts trade   

Tattoo discovered on ancient Egyptian mummy 

Scientists digitally unwrap mummy of Egyptian priest Neswaiu

Skull tower, a monument built along the road to Constantinople, served as a warning to anyone rising against the Ottoman Empire

Forensic anthropologist in El Salvador excavates and identifies victims of gang murders 

Shipwrecks archaeologists would love to find, from the Minoans to a shipwrecked Egyptian pharaoh 

Egyptian wine grape guard’s contract decoded   

Centuries-old grills of ancient BBQ lovers founding Turkey  

In Borneo, archaeologists are discovering vessels called “dragon jars” that sometimes contain bones of the dead 

Emperor Claudius dressed as pharaoh in newly uncovered carving 

The last taboo: what makes male humans and chimpanzees power hungry 

Quinnipiac students help investigate a possible Santeria ritual

Hey person in photo, that is not a right femur, why people need osteologists

Women in prehistory, who made this hand impression? 

Pre-Inca tomb discovered under the house of writer Mario Vargas Llosa  

Medical first: 3-D Printed skull successfully planted in woman 

Discoveries challenge beliefs on human arrival in the Americas 

Black death was airborne, not spread by fleas, research says 

Alaska’s real life “Bones” scientists puzzles out violence in ancient societies 

DNA sequencing of human remains paints a complicated picture of human evolution 

 

 

This week in anthropology, archaeology, bioarchaeology, biological anthropology, human evolution

Representation and perception of death in Neolithic Near East site Tell Qarassa examining funerary site, human image, and similar iconographic conventions

3 million year old fossil skeleton Little Foot (or Australopithecus prometheus) oldest most complete Australopithecus ever found; also believed to be oldest Homo skeleton found (see Archaeology Magazine and Science Now)

australopithecine “little foot”

New study shows that Native Americans and Russians share same language traits, dialects reveals how ancestors migrated 13,000 years ago 

Archaeologists want to explore human origins, Georgia wants to mine gold, which is worth more? 

Archaeologists tired of unearthing unspeakable ancient evils 

Billionaires with big ideas are privatizing American science 

1600 year old basilica dedicated to St Neophytus discovered in Turkey’s Lake Iznik architecturally similar to Hagia Sofia 

Burials in Greece linked to Macedonian kings 

Learn how archaeologists in the rural highlands of Peru are supporting the local schools by providing young boys and girls with opportunities (read more about the field school PIARA at the wordpress blog the Ancash Advocate)

Egyptians may have domesticated cats around 6,000 years ago based on cat skeletons found in cemetery, see also Live Science 

3200 year-old skeleton has oldest known example of cancer (metastatic carcinoma) associated with modern lifestyle  (such as environmental–carcinogens from wood fire smoke, genetic or from the parasite schistosomiasis), for more information see Archaeology Magazine and great photos visit Popular archaeology 

Graduate students should be encouraged to explore jobs outside academia and seek advice through campus career services 

Evolutionary fitness is not the most important determinant of success 

Classical archaeologist looks to shipwrecks and harbors to examine economic networks during Roman Empire 

“An anthropologists walks into a bar…” beer company hires social anthropologists to figure out why business is waning 

20+ skills that make PhDs employable 

Architecture analysis offers new clues to Petra’s culture 

Styloid process, an osteological genetic mutation that may have enabled humans to make tools, found in ancient fossil

Shocking facts from the scaffold 

Grad student deciphers 1800 year old letter from Egyptian solider 

What is plaque? 

Footless body with sheep bones discovered in UK 

Thinking more about teeth, dental anthropology

Study shows that race determines earwax scent

Why dark chocolate is good for your heart 

Cavities (tooth decay) causes, symptoms, and treatments 

Archaeologists use lasers to map site of Angkor, heart of SE Asia’s Khmer Empire 

Human nose can distinguish between a trillion smells

Amazon Warrior Women: Any truth behind the myth? 

High demand for underwater archaeology in Vietnam 

Conche shells evolved to be smaller because of hungry humans 

Vatican library to digitize its archive and put it online 

Epigenetics: the controversial science behind ethic and racial health disparities

Archaeologists are learning more about the Roman baths between Mġarr to Gћajn Tuffieћa in Malta 

A lot is known about Colonial India, but less about Ancient India 

Primatologists study infant chimps to get at root of gender differences in humans