Abstract:

Life-History Theory is a highly discussed topic in evolutionary biology. Important in an organism’s life are the evolutionary trade-offs that are made, such as deciding to attempt for one strategy over another. One influential life-history trait that often goes without discussion are immune system trade-offs. This review of the current literature on life-history of animal and human taxa focuses on the  trade-offs made between their immune systems and other integral systems and behaviors such as reproduction and individual survivorship. This review will offer information regarding experimental immune manipulation and immune system associated trade-offs across the animal kingdom. Further research in biological anthropology in the domain of human public health will allow for a greater scientific understanding of how human disease progresses and may offer insight to genetic pre-disposition to disease that is based off life-history tradeoffs and the environments that humans inhabit.

Introduction:

Life History is one of the most researched topics in the field of Evolutionary Biology. Trade-offs within individuals and populations of organisms determine how they adapt to ecological changes and constant drive to push their fitness to the limit. As the academic field of Evolutionary Biology has progressed, other academic disciplines have interpolated their studies to Life History, such as Evolutionary Anthropology and Evolutionary Psychology. In the last thirty years,  investigators have asked the question, “What trade-offs have humans and their ancestors made?” In human societies, we endure trade-offs on a fundamental level. Choices must be made about allocating financial resources, energy exertion, and reproductive choices. Social and natural scientists alike both have begun to ponder the connection of life-history trade-offs between humans and other animal taxa. Humans are unlike any insects, but both humans and animals endure the same basic trade-offs under the branches of survival-based and reproductive-based choices. One category of trade-offs that are often understudied are immunological trade-offs. These trade-offs mainly exist at a cellular level and impact the survivability of every organism. Immunological trade-offs may be intentional behaviors that impact daily decisions or may be carefully mediated, innate behaviors. Trade-offs between immunity and reproduction are often characterized in females, as they carry more reproductive behaviors than males, and males are less immunocompetent than females. This paper serves as a review of the current literature of immunological trade-offs in animal taxa and humans. This paper will also conclude with remarks of why life-history matters in humans, and how current immunologic tradeoffs may impact the species overall fitness.

 The history of Life History 

After Darwin, between 1910-1940, ideas started to emerge that each organism had a set of adaptive traits that were important for species evolution. (Stearns, 1976). Following this, between 1954 and 1973, there was a flurry of attempts to explain adaptive traits and evolution in a mathematical model. Of the many categories that were studied, it was found that reproduction and survivability were among the most clearly understood by mathematical function and correlational foundations of biology (Stearns, 1976). Shortly after, the field bloomed into what it is today  and started to intersect animal behavior with the environments around them (Stearns, 1976). At the heart of the foundation lies the basic trade-offs that are currently studied today. Energy is necessary for all organisms to survive and each organism has a limited amount of obtainable energy. Individuals must take the energy that they have obtained and allocate it towards their reproduction, competition with other individuals, and avoidance of predation (Cody, 1966). Not only do organisms have a limited amount of obtainable and usable energy, the amount of energy given to them is determined by the environment. 

In current Life History Theory, there are several different traits that an organism may choose to invest their energy and resources into. These categories can be broken down in two scales, the physiological trade-offs and evolutionary trade-offs (Schwenke et al., 2016). Physiological trade-offs arise as a consequence of physiological conflicts between two or more Life-history traits (Schwenke et al., 2016). For instance, if a choice must be made using the same limiting resource, this would constitute a physiological trade-off, such as opting for a larger body-size than an earlier age at sexual maturity. These types of trade-offs are plastic and mediated by environmental changes (Schwenke et al., 2016). Evolutionary trade-offs occur if individuals are pre-disposed to genetic traits that must be allocated preferentially. These trade-offs happen on a smaller and cellular scale and are often seen in immunity versus survival trade-offs (Schwenke et al., 2016). In humans, these trade-offs are similar yet different, as access to resources as a survivability trait is not foraging for food, rather than attaining financial resources to push their fitness forward.

 Trade-Off Basics

All living organisms face trade-offs between two or more different Life History Traits. Trade-offs are universal in the animal kingdom, but these trade-offs are individual specific. Evolutionary history is a culmination of several individuals making similar life-history trade-offs, and their fitness pushes their evolution forward. Individuals may opt to put more effort into their own survivability versus their reproduction. Individuals who place more energy into their own survival my attempt to attain more physical resources and this may extend their probability for successful life history choices in the future. However, investing early in traits does not necessarily ensure the individual a favorable outcome in their choice. Classical trade-offs, such as body size versus reproductive maturity, are canonically seen in classroom settings when discussing Life-history theory. Individuals may choose to invest higher in their survival, which consists of higher resource gathering and territory acquisition and defense. Individuals may also choose to invest higher in their reproduction,  including higher reproductive attempts with the opposite sex, higher copulations, or increased efforts in mate selection. Individuals may also opt to invest more in their immunity by placing energy or resources to directly affecting their immune defense. In humans, most of these choices are mediated through currency, as most humans live in societies where it is necessary to pay for food, housing (territory), health (immunity), or using those resources to attempt to attract a mate (reproduction). Inside of the immunity category, there is a choice between innate and acquired immunity. Innate immunity investment would be placing efforts into the antibodies’ and immune structures that were received through maternal transplantation. Acquired immunity may be from adoptive transfer of antibodies or through vaccination efforts.  

 Human Life History

Human Life-history theory is often covered by not only evolutionary biologists, but also evolutionary psychologists and other social scientists. Humans follow the type I survivorship curve and are characterized by having long lifespans with survivability dropping off the further they survive in the world. Humans are similar to animals in that they respond to their respective ecosystems by making trade-offs. Some unique morphological differences about humans compared to their primate ancestors is the presence of a large brain, which is between two to three standard deviations above the typical brain size/body size figures (Mace, 1981). Other differences include the following: expanded juvenile dependence, support of reproduction by older – post reproductive – individuals, male support of reproduction and offspring (Kaplan et al., 2000). Humans are also unique in that there is a use of a non-natural resource to directly influence their life histories – currency. Currency is what drives human societies and allows humans in most societies to accurately make choices between investments, such as reproduction, survival, and even immunity. Our understanding of Human life-history is reliant on the use of complex mathematics and psychological studies to predict the behavior of individuals and their life-history choices, but there is a great deal of information regarding the cellular-level trade-offs that occur between reproduction and immunity.

 Immunity Basics 

Individuals have two facets of immunity, innate and acquired. Innate immunity is passed down from mother to child either through the gestation of the child in the womb or via breast-feeding post birth. Antibodies and immune defense will be passed on physically through cellular copying into the child, but also through genetics. Children can be predisposed to the same genetic immunodeficiencies that may be active or dormant in the parents, such as diabetes, birth defects, and even cancers (Abbas et al., 2014). Acquired immunity is through facing a specific immune challenge and beating it. In humans, this can be accomplished through direct immune challenge or via vaccination. Direct immune challenge would be considered an acquiring of immunity if they face a disease that is novel to them, such as the flu. Acquired immunity can also be done through adoptive transfer of antibodies through vaccination (Abbas et al., 2014). This immunity is acquired as the body  faces new novel disease at a lower pathogenic load.

Humans have two different types of immunity, humoral and cell-mediated immunity (Abbas et al., 2014). Humoral immunity is mediated through recognition of the pathogen by B-cells. B Cells will produce antibodies that will attempt to link to the pathogen and inactivate them with specific receptors that are on the cellular membrane. These structures are non-specific for novel disease, but specific for recognized illness. In cell-mediated immunity, it is often non-specific invaders that come across T cells. These T-cells will actively increase in numbers about three to five days of pathogen recognition in the activation phase. After the pathogen is controlled, the cells are contract and enter the memory phase. There will be a higher count of memory T cells that will attack the pathogen if it is seen again in the immune system. Most other T cells will then enter the contraction phase and decrease in numbers due to T Regulator Cells mediating apoptosis through cellular membrane receptors.

 Reproduction vs. Immunity Tradeoffs in Non-Human Animals

Reproduction is among one of the highest life-history traits to be studied, as it gives scientists data regarding individual mating choices and strategies. One of the lesser studied fields within life-history theory is immunity. Immune functions are what drives individual survival on a cellular and molecular basis, and resource investment into this category is terminally important. Studying immunity gives insight in how to properly prepare for defense from an immune challenge and my offer insight into mechanisms of action in the progression of infectious disease across animal taxa. Individual organisms will opt to extend their genetic fitness into offspring and parental care and put their immunity at risk, or they will choose to have an extended life and forego several reproductive opportunities because the costs are too high. Evolutionary trade-offs between reproduction and immunity are often highlighted in female organisms, as they are most often the ones that must produce the offspring (Berglund, 2013). 

One taxon of organisms that make evolutionary trade-offs between immunity and reproduction are insects. Life-history trade-offs are more pronounced in organisms with relatively short lifespans, so their choices and traits are much more exaggerated (McDade, 2016). Reproductive processes can reduce or inhibit constitutive and induced immune function in some organisms (Schwenke et al., 2017). In a study with ground crickets – Allonemobius socius – it was seen that females had lower counts of hemocytes with increasing copulation frequency (Fedorka, 2004). While this was more pronounced in females more than males, both sexes had increased mortality with increased copulation (Fedorka, 2004). Male ground-crickets have higher concentrations of circulating hemocytes than females, and also have higher bacterial defense, but their immunity becomes compromised when offering a nuptial gift to the female, which requires extreme use of resources (Fedorka, 2004).

Additionally, immune function and choices can reduce or inhibit reproductive function. One of the most recognized trade-offs is seen in Drosophila melanogaster females and the hormones that they take in during copulation. The hormone that is taken in directly impacts their survivability, as the hormone is toxic to the body. Females will then inherently place more resources to somatic maintenance rather than reproductive opportunities, as the hormone changes their sexual libido. Additionally, pathogenic progression may change properties of individual’s reproductive allocations. By challenging Anopheles mosquitoes, the immune system begins to deteriorate the protein accumulation process in the reproductive organs (Ahmed & Hurd, 2006). Developed oocytes undergo their own random selection process of apoptosis, which is mediated by the pathogen progression, ultimately leading to a lower number of eggs laid post-copulation (Ahmed & Hurd, 2006).

In some lizard species, diet quality also affects investment, leaning further towards reproduction and immune defense. Increased immune response can take away energy use from other more energetically taxing functions, such as reproduction (Husak et al., 2016). It was unknown what conditions must be acted upon for there to be a cellular investment more in reproduction versus immune defense (Husak et al., 2016). In challenging lizards with different types of dietary restrictions, they were trying to see if an investment in reproduction was capable to switching to immune defense, as lacking nutrition causes lower defense in immune function (Husak et al., 2016). After fishing the challenge, both immune function and reproduction  decreased at the same rate among the population (Husak et al., 2016). However, there were individuals that invested more in immune defense and reproduction, as there were increased immune cell counts as well as increased hormone production in different groups (Husak et al., 2016). Differential counts of growth/reproduction hormones relative to immune cell counts is not uncommon. When studying simpler immune systems, male Gryllus texensis will opt for lower immunocompetence rather than reproduction (Adamo et al., 2001). Resources were put towards reproductive courting behaviors and there were lower phenoloxidase activity along with lower susceptibility to bacterial immune challenge (Adamo et al., 2001). It is clear that some individuals will opt for higher hormone counts versus cellular defense. This lack in defense will cause lower counts of damaging parasitic load and faster disease progression in most organisms. 

 Human Immunity vs Reproduction

Humans can also undergo the same reproduction/immunity trade-offs that animal taxa endure. In human gestation, the body goes through an extreme amount of energy loss in other bodily functions to build the child in the womb. Not only is energetic effort directed toward child development, but this is also a time-consuming expenditure. Like insects, mostly women face the trade-offs between immunity and reproduction, as both immune defense and childbearing are heavy-weighing functions in their life history. By adulthood, both male and female immune function have stark contrasts, such as lower immunocompetence in males (Abrams & Miller, 2011). When a woman contracts an infectious disease during their reproductive process, the body must shift its resources over to host defense (Abrams & Miller, 2011). Additionally, with the loss of bodily function directed to bearing the child, the resource allocation process can shift to different patterns of resource gathering and allocation. 

As humans age, there is a stark decrease in immune investment and a increase in reproductive investment. The number of TCells , BCells,, and antibodies decrease with age progression along with Helper T and Suppressor T proliferation decreases (McDade, 2003). Additionally, the development of human mating systems, including hormones, does not occur until around the ages of ten and twelve in most adolescents (McDade, 2003). Because of this, there is a shift in investment towards the reproductive systems over immunity. It is speculated that numbers of immune cells and processes drop as time increases, due to risk of death lowering with higher immunocompetence (McDade, 2003). Hormones can influence the immune system due to the dimorphic nature of the immune and reproductive systems in humans. 

Females bear the load of breast-feeding their offspring, and this allows for proteins to be transferred directly from mother to child easily. The placenta is replaced by breastmilk as the child’s direct source of nutrition and passive immunity, and also strengthens the child for up to six months post-birth (McDade, 2003). Those that choose to breast-feed their children pass on the benefits of being able to survive basic immune challenges for a short duration of their life, but at a cost. While antibodies are being reproduced and sent to the child through the breastmilk, the immune system is constitutively active and expending energy instead of allocating it (McDade, 2003). 

The development of menopause in female humans sets their reproductive life-histories apart from other sexually reproducing organisms. Menopause is defined as the loss of fertility in female humans (Shanley & Kirkwood, 2001). In evolutionary biological, the progression and evolution of menopause is a puzzling phenomenon. There are several different theories that may have allowed for the progression of menopause to happen, although no one theory reins true. As a female age, there is a sharp rise in estradiol but a decline in immune function. It is hypothesized by Shanley & Kirkwood that the loss of reproductive function is due to investment in immune function in later stages of life (2001). There is also an increased maternal mortality during reproduction as reproductive behaviors enter into the later stages of reproduction. It is also speculated via mathematical models that the use of post-reproductive individuals may help increase inclusive kin fitness as a currently pregnant mother enters the childbearing stages (Shirley & Kirkwood, 2001).  No significant results were presented in this composite model study, however these results were not tested in any populations. Their study suggests that menopause is a process that is extremely complex and that adult mortality is taken into account for the progression of menopause (Shirley & Kirkwood, 2001).

Women also expend energy in other reproductive means. Menopause is caused by hormonal and egg-mediated changes in their reproductive system and takes away energy from them, but the advent of rearing offspring is extremely energy draining. While it is unknown the actual caloric needs to properly rear offspring from a single female individual, scientists are able to predict the energy requirements from birth and adolescence survival rates. Retroactive studies can be done in large populations of individuals and analyze population changes through birth and death certificates. 

One study that was able to hypothesize energetic changes among females was done by Lummaa et al in 2001. Lummaa analyzed humans in two ecologically different areas of Finland between 1752 and 1850. This society was pre-industrial, which gives an accurate depiction of true human life-history informatics (Lummaa et al., 2001). Humans sometimes rear more than a singleton offspring and was selected against in the past under the most favorable conditions (Kaukioja et al., 1989). In other mammals, rearing more than a single child is uncommon, as larger organisms with longer gestation periods require more energy. It is also known that there is a biased male morbidity and mortality in other mammals under stressful conditions (Stinson, 1985). It was found that fitness off twin offspring was dependent on the gender (Lummaa et al., 2001). Increasing litter-size from singleton offspring to duple and triple offspring resulted in loss of fitness in offspring (Lummaa, 2001). There was a drop in offspring survival as inclusive litter count increased, as offspring following singleton or duplum reproductive events had lower fitness (Lummaa et al., 2001). Additionally, there was a male bias in morbidity and mortality post-birth, showing a potential energetic formation bias to singleton females over singleton males and twins (Lummaa et al., 2001).

Human energy expenditure in current industrialized societies is  limited to our physiological size. Humans also have variable energetic rates that are determined through our physiological size and physical fitness. A human that is physically fit and lean in size has more available energy than a human that is not physically fit and overweight. Making the energetic investment in immune function versus reproduction in industrial humans is different because our access to mortality-altering properties such as vaccines is unique. In an analysis of current industrial society, we do see life expectancy rates drop off with rates, but differing energetic costs per condition.  Reproductive rates drop in conjunction with immunological load and with age in humans (Burget et al., 2011). Additionally, energetic use increases with age and among first reproduction and menopause (Burger et al., 2011). Humans that must make the choice between investing more in immune function versus their life-expectancy and reproduction. The choices that are made may alter future probabilities of successful tradeoffs, such as increased inclusive fitness when investing more in immunity versus fast birth of offspring.

 Are Humans Different Than Animals?

Humans and animals both endure similar trade-offs and follow the same life curves that are proposed to animal populations, but are these two different types of organisms different than one another in an evolutionary standpoint? The answer to that depends on who answers this question, as there is evidence for both arguments. Humans can be considered an animal in the context of evolutionary biology because they do in fact share the same environment with animal taxa. Humans, however, only built the environment around us as a way of living, like termite towers. Humans follow the same selection mechanisms as well. Fundamentally, humans follow the same life cycle as animal taxa, birth, proliferation, reproduction, and death (Balbontin et al., 2003). The selection hypothesis poses that natural selection processes increase with age in better quality individuals than lower quality individuals (Balbontin et al., 2003). Humans also have similar immunological systems to animals with similar types of cells and processes (Abbas et al., 2007). Most of human immunological research is conducted in mice, swine, and other mammals. If we follow the same life changes, share biological and genotypic similarities, and face the same life history traits, are we not animals to begin with?

The answer isn’t as clear cut. While humans do follow similar trends to domesticated and wild animals, they also are the reason why some ecological trends exist. Humans have increased their adaptability to the environment as years have gone on with increased longevity, forward planning, larger encephalization quotients, and greater family stability (Gottfredson, 1994). Vertebrates have a wide variety of sexual reproduction methods, but one unique aspect is that in nearly all animal species does fecundity reach a zero like in humans (Vomsaal et al., 1994). This decrease in humans is characteristic of other mammals who may have evolutionarily be selected for higher immunity and survival over further reproduction, but older mammals may still reproduce as a terminal investment (Vomsaal et al., 1994). Humans and animals do encounter novel changes in their respective environments, such as climate and predation, but most animal interactions with humans are often mediated through the presence of humans. It is not common to see speciation occur due to an urban environment or a new environment that was entirely created by humans. These negative interactions bring forth vast ecological change for human benefit, leaving humans facing the trade-off of human preservation of life or human consumption of life (Balbontin et al., 2003). 

 Why Life History Theory & Immunology Matters

The innervation of Immunology into evolutionary biology is a must for the discipline to continue forward. The immunological trade-offs that exist matter in the context of survivability and reproduction. Trade-offs can be made through innate and acquired immunity to affect future trade-offs. Individuals may invest in more immune defense if the environment is full of pathogens, such as humans. Most humans will opt to vaccinate themselves and their children at birth to give them a better option at survivability. Those who forego vaccination processes in their children will often see their children’s life expectancies to be much shorter than adolescents in their cohort. It is often seen that humans who do not vaccinate themselves against communicable and treatable disease will die from treatable diseases. Immunity is a difficult type of trade-off to study, as it requires extensive analysis through complicated machinery. These trade-offs can be understood on a cellular fundamental level through blood analysis while an organism is alive or dead. This process is expensive and requires flow-cytometry to produce numbers of cells.

It is important that life-history and immunology is studied further. While there is no direct say in how humans and animal taxa are inherently related, they do have similarities in cellular structure and disease progression. Both humans and animal taxa face similar trade-offs, however these trade-offs may be mediated differently. Predation in humans may be genetic factors, or they may be through predation from other organisms. Studying Life-history theory is an important part of biological and psychological science. Studying the behaviors of individuals may allow for conclusions to be made about their individual versus group behaviors. Studying Life-history also gives insight into evolutionary trade-offs that are being selected for in populations. This information allows scientists to understand what decisions are contributing to a higher fitness not just in the animal kingdom, but in humans as well. Human Life-history Theory in a broad sense allows us to understand what evolutionary strategies exist within our own behaviors, such as resource acquisition, mate selection, and social choices. If not for life history theory, would we know what choices are most important for human and animal survival? The answer is unknown at the time, but studying theory allows for us to attempt to find those answers.

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