Himalayas

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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