The Evolution of Human Reproduction in Parasite Stressed Environments
by Hansika Behl, Genetics
Abstract: This research synthesis investigates the evolutionary impact of parasitic stress on human populations, exploring the underlying mechanisms and outcomes related to reproduction, birth weight, and offspring sex ratios. Parasitic diseases, like malaria and polyparasitism, pose global health risks, with varying impacts on populations. The paper reveals correlations between parasitic environments and heightened fertility, altered birth weights, and skewed offspring sex ratios. The evolutionary response to parasitic stress is complex, with conflicting evidence on the production of costlier, larger offspring. It is concluded that although parasites may indeed increase reproductive investment in offspring, this may solely represent the number of offspring produced, making it plausible that the observed increase in offspring produces largely females due to their lower investment requirements by mothers. It is important to consider these variances in human sex ratios because they can result in changes in the dynamics of human communities, including mate choice, societal roles, and gender expectations.
parasites, evolution, birth weight, human reproduction, mate choice
Environments With Parasite Stress
Parasites impair healthy development worldwide, posing serious risks of illness and death to human populations. These include parasites that commonly infect humans, as well as those that rarely do but can still induce serious diseases if left untreated or wrongly diagnosed (Chomicz et al., 2016). For instance, malaria, a parasitic disease vectored by Anopheles mosquitoes, is a global health burden, with an estimated 229 million cases reported worldwide in 2019 (Fikadu & Ashenafi, 2023). Clinical diagnosis is often inaccurate due to symptoms resembling other tropical diseases. Artemisinin, an effective treatment, faces resistance, with resistant strains first reported in 2008 and spreading to Southeast Asia (Fikadu & Ashenafi, 2023).
Furthermore, polyparasitism, infection with multiple parasite species, is common in modern populations. Coinfection occurs in 1-10% of malaria cases, even where Plasmodium falciparum, the parasite that causes malaria, predominates (Murray & Bennett, 2009). In West Africa, three-quarters of the population harbored three or more parasites concurrently, including Plasmodium falciparum, Schistosoma haematobium, Schistosoma mansoni, and hookworm (Raso et al., 2004). Polyparasitism leads to more intense symptoms and infections, increasing susceptibility to other diseases (Pullan & Brooker, 2008). The effects of polyparasitism on humans have been observed to be extreme, with studies showing deficiencies in nutrition due to mechanisms such as anorexia, chronic blood loss, and malabsorption. This nutritional decline also affects human growth and organ pathology, causing hepatosplenic interactions in children (Pullan & Brooker, 2008). The age-profiles of polyparasitism indicate that pregnant women and school-aged children are at the highest risk of infection (Pullan & Brooker, 2008).
From an evolutionary perspective, human mothers, like other mammals, aim to maximize reproductive success by having fit offspring relative to their environments (Thomas et al., 2004). Risks such as chronic somatic diseases, environmental conditions, and infectious diseases can reduce fitness, driving the evolution of traits that promote increased fitness in populations.
The presence of parasites in human populations poses significant risks of illness and death, prompting evolutionary changes to combat susceptibility. These changes may affect patterns of sexual selection, leading to potential impacts on mate choice and sexual dimorphism. Studying these evolutionary changes can provide insight into defining characteristics of populations most at risk in parasite-stressed environments, guiding therapies to increase lifespans and fitness. These findings can also inform strategies for newly emergent pathogens, reducing their detrimental effects on humans.
Effects of Parasite Stress on Human Reproduction
Parasitic diseases have had a major impact on human population demography around the world, but focus has generally centered around mortality rates, rather than the effects on human biology and short and long-term fitness consequences of parasite stress. The degree of parasitism in an environment is a key ecological factor that influences the condition of parents, which affects the fitness of their offspring (Dama, 2012). To counteract this existence of parasites, hosts have been found to respond by adjusting their life-history traits, which include traits related to the survival and reproduction of an individual in one life-span, such as birth weight, number of offspring, and age of maturity. In the case of human reproduction specifically, hosts have been observed to adjust their reproductive biology by increasing reproductive output and/or reducing age at maturity (Dama, 2012). These shifts in reproduction parameters may be consolidated by genetic change or phenotypic plasticity, but few studies have focused on uncovering how these parasitic environmental factors explain variability in life-history (Guégan et al., 2001).
Parasite stress can have several evolutionary impacts on human populations. It can deteriorate the body condition of parents by reducing nutrient absorption and investing in defense mechanisms at the cost of other physiological processes (Pullan & Brooker, 2008; Dama, 2012), hindering the mother’s ability to invest in costlier offspring. Conversely, infants with lower birth weights are at a higher risk of developing diseases, suggesting an evolutionary shift towards mothers producing larger offspring (Thomas et al., 2004). Parasites can also affect human lifespan, potentially leading mothers to reach reproductive maturity earlier and produce more children over their lifespan, thus increasing their fertility (Guégan et al., 2001). While these studies generally agree on the evolutionary effect of parasitic environments on human reproduction, there appear to be conflicting conclusions regarding the scope of these effects.
An agent-based model was used to simulate the process of evolutionary selection on life history strategy by analyzing data from 89 countries worldwide, encompassing diverse geographic, cultural, and economic regions. Data was collected for a set of 16 categories of human diseases known to affect human survival, with 5 of those being parasitic diseases, including malaria, schistosomiasis, filariasis, dracunculiasis, and trypanosomiasis. It was found that if the parasite stress component is superior to the environmental stress, the human birth weight monotonically rises, meaning it may stay constant but it never increases (Thomas et al., 2004). A nonmonotonic relationship was also identified between the number of infections and birth weight, with birth weight reaching its lowest from 8-10 infections, and then increasing with more infections (Thomas et al., 2004).
A similar relationship was seen with the fertility of mothers by using a general linear model to look at the direct effect of parasitic and infectious disease agent species across 150 countries worldwide. Spatial factors, including total area, mean latitude, mean longitude, hemisphere (Northern or Southern), and whether the country was located on the mainland or an island, were taken into consideration. Additionally, the predominant religious groups in each country were accounted for to address potential cultural and social influences on human fertility and disease diversity. Data was compiled from 16 categories of human diseases known to have significant effects on human health, with 7 of those being parasitic diseases, including malaria, schistosomiasis, filariasis, dracunculiasis, Chagas disease, cutaneous leishmaniasis, and visceral leishmaniasis. The mean human female fertility, defined as the number of offspring born per woman aged 15–44 years, was significantly positively correlated with the parasite and infectious disease species present in the environment (p-value = 0.006), when all other influential environmental, demographic, and socioeconomic factors were controlled for (Guégan et al., 2001).
A significant negative relationship was found between parasite stress, measured as Disability-adjusted Life Years (DALY), and the offspring sex ratio at birth (SRB), which is the ratio of male births to female births (p-value = 0.007) (Dama, 2012). This relationship was identified through an analysis of data from 226 countries, which were grouped into tropical and temperate zones for analysis. DALY combines years of life lost due to premature mortality and years lived with disability, providing a comprehensive assessment of the burden of parasitic diseases on health within populations. Although the specific parasites were not explicitly detailed in the study, this measure encompasses disability resulting from 28 important parasites.
Since males are larger in size, they require higher investment by mothers. Therefore, it is plausible that a parasite-stress-dependent environment constrains the ability of mothers to invest in male offspring. This finding contradicts the correlation of increasing birth weights and parasite stress observed earlier (Thomas et al., 2004). Interestingly, this study also noted a negative relationship between fertility levels and the offspring SRB (p = 0.047), indicating that higher fertility levels produce fewer male offspring (Dama, 2012).
Research indicates that parasitic stress in environments has a positive correlation with both fertility and birth weight, but negative correlations with producing costlier, larger offspring. This pattern of results suggests that further research may be necessary to determine whether parasitic stress is a cause of these evolutionary effects in human reproduction, and whether this effect is related to the selection of larger or smaller children. However, it should be noted that Dama’s (2012) study was completed more recently than the other two, with about a 10 year gap. Although 10 years is not one full human generation, so it is likely not enough time to conclude evolutionary change in birth weight over time, it is indicative of variability between the studies and may even suggest that differing environmental conditions exerted varying pressure at differing times.
Factors that Contribute to the Evolution of Birth Weight
Research indicates that the evolution of birthweight in a parasitic environment stems from different factors. Previous research has indicated that mathematical models in which virulence evolves in response to host reproduction have a positive association, showing that there could be causation between fertility and parasitism (Hochberg et al., 2000). This conclusion can be supported by the significant positive correlation between human fertility and parasitic environments (Guégan et al., 2001). This relationship suggests an increase in reproductive investment in offspring that are more likely to survive and reproduce in such environments. Since children with lower birth weights tend to be more susceptible to infections, selection seems to favor children with higher birth weights in high infection environments (Thomas et al., 2004). Additionally, once a threshold of infection risk is exceeded in an environment, birth weights significantly increase (Thomas et al., 2004). This further supports the claim that extreme environments favor higher birth weights.
However, parasites also result in substantial deterioration of body condition (World Health Organization, 2004), which affects the conditions of the parents to reproduce. Although there is evidence for increased fertility in parasitic environments (Guégan et al., 2001), it is plausible that this increase in fertility does not account for the characteristics of the offspring that are produced by females. In fact, a negative correlation is seen between high fertility and offspring SRB, indicating that an increase in fertility does not correlate to the ability of mothers in parasite-rich environments to produce costlier, larger offspring. Thus, the higher nutrition investment required by mothers to produce males over females is a possible reason why offspring are largely females in environments with high parasite numbers (Dama, 2012). A similar phenomenon was also seen in birds with parasite stressed environments constraining the ability of parents to invest in sons, which are the costlier offspring (Reed et al., 2008). This suggests that the effect of parasites on selection of gender is relatively conserved and may be a plausible explanation for the observed data.
Although parasites may indeed increase reproductive investment in offspring, this may solely represent the number of offspring produced. Considering the evidence seen in offspring SRB (Dama, 2012), it is plausible that the observed increase in offspring (Guégan et al., 2001) produces largely females due to their lower investment requirements by mothers. It could be concluded that higher fertility does not indicate the ability to invest in offspring that require higher investment. The SRB variance is important in evolution because higher numbers of females can lead to strong sexual selection among females, which can lead to sexual dimorphism.
Further Research
Establishing Causation
Although the discussed patterns in human fertility, birthweight, and SRB have been observed relative to parasite stressed environments (Thomas et al., 2004; Guégan et al., 2001, Dama 2012), causation cannot be established with these tested models. Controlled studies need to be done that establish constant environments and control for any extrinsic factors, rather than the observational studies discussed in this paper. The results of these controlled studies can be used to establish causation between the observed evolutionary changes and parasite stress in environments. However, it can be difficult to establish causation in human evolutionary studies because models can only look at previous data and trends in human reproduction, since it is not very feasible or ethical to conduct large, controlled experiments with humans over generations.
Weighing the Individual Effects of Other Pathogens
Many studies in this paper tend to combine the effects of human parasitic and infectious diseases into a single category, as shown in the works of Thomas et al. (2004) and Guégan et al. (2001). By grouping parasitic, bacterial, and viral infections together, the unique impacts of each type of pathogen are often overlooked. It is conceivable that certain pathogens may exert greater selective pressure than others, leading to varying levels of evolutionary change in human reproduction. To identify such trends, studies that individually compare the effects of parasites, bacteria, and viruses on human health and evolution are necessary. These findings can help establish the extent of evolutionary changes in humans based on the types of pathogens present in their environment.
Evolutionary Trade-Offs
In the discussed studies, it is assumed that the change in human reproduction is a response to parasite-linked fitness. However, the alternative hypothesis that this change in reproductive budget is invested in multiple dimensions of reproductive output, such as size and number of offspring, is to counter diminishing returns in any one dimension of investment cannot be excluded (Thomas et al., 2004). Further research needs to be conducted to understand the trade-offs between fertility, offspring size, and offspring number, in relation to different scenarios of infection exposure. Such results will provide evidence to whether the evolution of human reproduction is a direct result of parasite stress to improve fitness or if there is a component of reproduction that is diminished as a result.
Distinguishing between Evolutionary Mechanisms
The discussed studies assert that change in human reproduction due to parasite stress is present, but the specific mechanisms of these changes still remain relatively unknown. Further research needs to be done to directly test the birth weight of children, as well as the SRB, to see whether the observed conclusions made in this paper between the referenced studies are in fact true. Additionally, further research needs to be done to understand the scope of the impact of increased fertility and birth weight. It is still unclear whether an increase in fertility is a product of women reaching reproductive maturity earlier or producing more total children in the same or shorter reproductive lifespan in parasite stressed environments. It is also unclear whether the conclusion that an increase in human fertility in parasite stressed environments increases the number of offspring, but reduces the ability to produce costlier offspring is true, or if the contradiction of these relationships is simply due to variability between the discussed studies.
References
Chomicz L., Conn, D., Szaflik, J., and Szostakowska, B. 2016. Newly emerging parasitic threats for human health: National and international trends. BioMed Research International, 2016. 10.1155/2016/4283270
Dama, S. M. 2012. Parasite stress predicts offspring sex ratio. Plos One, 7(9), e46169. https://doi.org/10.1371/journal.pone.0046169
Fikadu, M., & Ashenafi, E. 2023. Malaria: An overview. Infection and Drug Resistance, 16, 3339–3347. https://doi.org/10.2147/IDR.S405668
Guégan, J.F., Thomas, F., Hochberg, M. E., Meeus, T. de, and Renaud, F. 2001. Disease diversity and human fertility. Evolution, 55(7), 1308–1314. doi:10.1111/j.0014-3820.2001.tb00653.x
Hochberg, M. E., Gomulkiewicz, R., Holt, R.D., and Thompson, J.N. 2000. Weak sinks could cradle mutualisms: strong sources should harbour pathogens. Journal of Evolutionary Biology, 13, 213–222.
Murray, C. K., and Bennett, J. W. 2009. Rapid diagnosis of malaria. Interdisciplinary Perspectives on Infectious Diseases, 2009, 415953. https://doi.org/10.1155/2009/415953
Pullan, R., and Brooker, S. 2008. The health impact of polyparasitism in humans: Are we under-estimating the burden of parasitic diseases? Parasitology, 135(07). 10.1017/s0031182008000346
Raso, G., Luginbühl, A., Adjoua, C. A., Tian-Bi, N. T., Silué, K. D., Matthys, B., Vounatsou, P., Wang, Y., Dumas, M. E., Holmes, E., Singer, B. H., Tanner, M., N’goran, E. K., and Utzinger, J. (2004). Multiple parasite infections and their relationship to self-reported morbidity in a community of rural Côte d’Ivoire. International Journal of Epidemiology, 33(5), 1092–1102. https://doi.org/10.1093/ije/dyh241
Reed T.E., Daunt, F., Hall, M.E., Phillips, R.A., and Wanless, S. 2008. Parasite treatment affects maternal investment in sons. Science, 321, 1681–1682.
Thomas, F., Teriokhin, A.T., Budilova, E.V., Brown, S.P., Renaud, F. and Guegan, J.F. 2004. Human birthweight evolution across contrasting environments. Journal of Evolutionary Biology, 17: 542-553. https://doi.org/10.1111/j.1420-9101.2004.00705.x
World Health Organization. 2004. The World Health Report. Geneva: World Health Organization.
Acknowledgements: I gratefully acknowledge Dr. Tessa Andrews and Writing Coach Ben Jackson for their help with providing very detailed revisions and suggestions to this paper, and encouraging me to share my work with other readers.
Citation Style: Nature