Parental investment

From Wikipedia, the free encyclopedia

https://en.wikipedia.org/wiki/Parental_investment 

A female calliope hummingbird feeding her chicks

A human mother feeding her child

Parental investment, in evolutionary biology and evolutionary psychology, is any parental expenditure (e.g. time, energy, resources) that benefits offspring. Parental investment may be performed by both males and females (called biparental care), females alone (exclusive maternal care) or males alone (exclusive paternal care). Care can be provided at any stage of the offspring's life, from pre-natal (e.g. egg guarding and incubation in birds, and placental nourishment in mammals) to post-natal (e.g. food provisioning and protection of offspring).

Parental investment theory, a term coined by Robert Trivers in 1972, predicts that the sex that invests more in its offspring will be more selective when choosing a mate, and the less-investing sex will have intra-sexual competition for access to mates. This theory has been influential in explaining sex differences in sexual selection and mate preferences, throughout the animal kingdom and in humans.

History

Sexual selection is an evolutionary concept that has been used to explain why, in some species, male and female individuals behave differently in selecting mates. In 1930, Ronald Fisher wrote The Genetical Theory of Natural Selection, in which he introduced the modern concept of parental investment, introduced the sexy son hypothesis, and introduced Fisher's principle.

In 1948, Angus John Bateman published an influential study of fruit flies in which he concluded that because female gametes are more costly to produce than male gametes, the reproductive success of females was limited by the ability to produce ovum, and the reproductive success of males was limited by access to females. In 1972, Robert Trivers continued this line of thinking with his proposal of parental investment theory, which describes how parental investment affects sexual behavior. He concluded that whichever sex has higher parental investment will be more selective when choosing a mate, while the sex with lower investment will compete intra-sexually for mating opportunities. In 1974, Trivers extended parental investment theory to explain parent–offspring conflict, the conflict between the amount of investment that is optimal from the parent's perspective, versus from the offspring's perspective.

Parental care

Main article: Parental care

Parental investment theory is a branch of life history theory. The earliest consideration of parental investment is given by Ronald Fisher in his 1930 book The Genetical Theory of Natural Selection, wherein Fisher argued that parental expenditure on both sexes of offspring should be equal. Clutton-Brock expanded the concept of parental investment to include costs to any other component of parental fitness.

Male dunnocks tend to not discriminate between their own young and those of another male in polyandrous or polygynandrous systems. They increase their own reproductive success through feeding the offspring in relation to their own access to the female throughout the mating period, which is generally a good predictor of paternity. This indiscriminative parental care by males is also observed in redlip blennies.

A cellar spider defending spiderlings.

In some insects, male parental investment is given in the form of a nuptial gift. For instance, ornate moth females receive a spermatophore containing nutrients, sperm and defensive toxins from the male during copulation. This gift, which can account for up to 10% of the male's body mass, constitutes the total parental investment the male provides.

In some species, such as humans and many birds, the offspring are altricial and unable to fend for themselves for an extended period of time after birth. In these species, males invest more in their offspring than do the male parents of precocial species, since reproductive success would otherwise suffer.

The benefits of parental investment to the offspring are large and are associated with the effects on condition, growth, survival, and ultimately on reproductive success of the offspring. For example, in the cichlid fish Tropheus moorii, a female has very high parental investment in her young because she mouthbroods the young and while mouthbrooding, all nourishment she takes in goes to feed the young and she effectively starves herself. In doing this, her young are larger, heavier, and faster than they would have been without it. These benefits are very advantageous since it lowers their risk of being eaten by predators and size is usually the determining factor in conflicts over resources. However, such benefits can come at the cost of parent's ability to reproduce in the future e.g., through increased risk of injury when defending offspring against predators, loss of mating opportunities whilst rearing offspring, and an increase in the time interval until the next reproduction.

A special case of parental investment is when young do need nourishment and protection, but the genetic parents do not actually contribute in the effort to raise their own offspring. For example, in Bombus terrestris, oftentimes sterile female workers will not reproduce on their own, but will raise their mother's brood instead. This is common in social Hymenoptera due to haplodiploidy, whereby males are haploid and females are diploid. This ensures that sisters are more related to each other than they ever would be to their own offspring, incentivizing them to help raise their mother's young over their own.

Overall, parents are selected to maximize the difference between the benefits and the costs, and parental care will be likely to evolve when the benefits exceed the costs.

Parent-offspring conflict

Main article: Parent–offspring conflict

Reproduction is costly. Individuals are limited in the degree to which they can devote time and resources to producing and raising their young, and such expenditure may also be detrimental to their future condition, survival, and further reproductive output. However, such expenditure is typically beneficial to the offspring, since it enhances their condition, survival, and reproductive success. These differences may lead to parent-offspring conflict. Parents are naturally selected to maximize the difference between the benefits and the costs, and parental care will tend to exist when the benefits are substantially greater than the costs.

Parents are equally related to all offspring, and so in order to optimize their fitness and chance of reproducing their genes, they should distribute their investment equally among current and future offspring. However, any single offspring is more related to themselves (they have 100% of their DNA in common with themselves) than they are to their siblings (siblings usually share 50% of their DNA), so it is best for the offspring's fitness if the parent(s) invest more in them. To optimize fitness, a parent would want to invest in each offspring equally, but each offspring would want a larger share of parental investment. The parent is selected to invest in the offspring up until the point at which investing in the current offspring is costlier than investing in future offspring.

In iteroparous species, where individuals may go through several reproductive bouts during their lifetime, a tradeoff may exist between investment in current offspring and future reproduction. Parents need to balance their offspring's demands against their own self-maintenance. This potential negative effect of parental care was explicitly formalized by Trivers in 1972, who originally defined the term parental investment to mean "any investment by the parent in an individual offspring that increases the offspring's chance of surviving (and hence reproductive success) at the cost of the parent's ability to invest in other offspring".

King penguin and a chick

Penguins are a prime example of a species that drastically sacrifices their own health and well-being in exchange for the survival of their offspring. This behavior, one that does not necessarily benefit the individual, but the genetic code from which the individual arises, can be seen in the King Penguin. Although some animals do exhibit altruistic behaviors towards individuals that are not of direct relation, many of these behaviors appear mostly in parent-offspring relationships. While breeding, males remain in a fasting-period at the breeding site for five weeks, waiting for the female to return for her own incubation shift. However, during this time period, males may decide to abandon their egg if the female is delayed in her return to the breeding grounds.

It shows that these penguins initially show a trade-off of their own health, in hopes of increasing the survivorship of their egg. But there comes a point where the male penguin's costs become too high in comparison to the gain of a successful breeding season. Olof Olsson investigated the correlation between how many experiences in breeding an individual has and the duration an individual will wait until abandoning his egg. He proposed that the more experienced the individual, the better that individual will be at replenishing his exhausted body reserves, allowing him to remain at the egg for a longer period of time.

The males' sacrifice of their body weight and possible survivorship, in order to increase their offspring's chance of survival is a trade-off between current reproductive success and the parents' future survival. This trade-off makes sense with other examples of kin-based altruism and is a clear example of the use of altruism in an attempt to increase overall fitness of an individual's genetic material at the expense of the individual's future survival.

Maternal-offspring conflict in investment

The maternal-offspring conflict has also been studied in animals species and humans. One such case has been documented in the mid-1970s by ethologist Wulf Schiefenhövel. Eipo women of West New Guinea engage in a cultural practice in which they give birth just outside the village. Following the birth of their child, each woman weighed whether or not she should keep the child or leave the child in the brush nearby, inevitably ending in the death of the child. Likelihood of survival and availability of resources within the village were factors that played into this decision of whether or not to keep the baby. During one illustrated birth, the mother felt the child was too ill and would not survive, so she wrapped the child up, preparing to leave the child in the brush; however, upon seeing the child moving, the mother unwrapped the child and brought it into the village, demonstrating a shift of life and death. This conflict between the mother and the child resulted in detachment behaviors in Brazil, seen in Scheper-Hughes work as "many Alto babies remain[ed] not only unchristened but unnamed until they begin to walk or talk", or if a medical crisis arose and the baby needed an emergency baptism. This conflict between survival, both emotional and physical, prompted a shift in cultural practices, thus resulting in new forms of investment from the mother towards the child.

Alloparental care

Alloparental care also referred to as 'Allomothering,' is when a member of a community, apart from the biological parents of the infant, partake in offspring care provision. A range of behaviors fall under the term alloparental care, some of which are: carrying, feeding, watching over, protecting, and grooming. Through alloparental care stress on parents, especially the mother, can be reduced, therefore reducing the negative effects of the parent-offspring conflict on the mother. The apparent altruistic nature of the behavior may seem at odds with Darwin's theory of natural selection, as taking care of offspring which are not one's own would not increase one's direct fitness, while taking time, energy and resources away from raising one's own offspring. However, the behavior can be explained evolutionarily as increasing indirect fitness, as the offspring is likely to be non-descendent kin, therefore carrying some of the genetics of the alloparent.

Offspring and situation direction

Parental investment behavior enhances the chances of survival of offspring, and it does not require underlying mechanisms to be compatible with empathy applicable to adults, or situations involving unrelated offspring, and it does not require the offspring to reciprocate the altruistic behavior in any way. Parentally investing individuals are not more vulnerable to being exploited by other adults.

Trivers' parental investment theory

Parental investment as defined by Robert Trivers in 1972 is the investment in offspring by the parent that increases the offspring's chances of surviving and hence reproductive success at the expense of the parent's ability to invest in other offspring. A large parental investment largely decreases the parents' chances of investing in other offspring. Parental investment can be split into two main categories: mating investment and rearing investment. Mating investment consist of the sexual act and the sex cells invested. The rearing investment is the time and energy expended to raise the offspring after conception. In most species, the female's parental investment in both mating and rearing efforts greatly surpasses that of the male. In terms of sex cells (egg and sperms cells), the female's investment is typically a larger portion of both genetic material and overall virility, while typically males produce thousands of sperm cells on a daily basis. Trivers' believed that this theory explained sexual jealousy. A criticism of the theory comes from Thornhill and Palmer's analysis of it in A Natural History of Rape: Biological Bases of Sexual Coercion, as it seems to rationalise rape and sexual coercion. Thornhill and Palmer claimed rape is an evolved technique for obtaining mates in an environment where women choose mates. As PIT claims males seek to copulate with as many fertile females as possible, the choice women have could result in a negative effect on the male's reproductive success. If women did not choose their mates, Thornhill and Palmer claim there would be no rape. This ignores a variety of sociocultural factors, such as the fact that not only fertile females are raped – 34% of underage rape victims are under 12, which means they are not of fertile age, thus there is no evolutionary advantage in raping them. 14% of rapes in England are committed on males, who cannot increase a man's reproductive success as there will be no conception. Trivers' theory does not account for women having short-term relationships such as one-night stands, and that not all men behave promiscuously. An alternative explanation to parental investment theory and mate preferences would be Buss and Schmitt's sexual strategies theory.

Human parental investment

Human women have a fixed supply of around 400 ova, while sperm cells in men are supplied at a rate of twelve million per hour. Also, fertilization and gestation occur in women, investments which outweigh the man's investment of a single effective sperm cell. Furthermore, for women, one act of sexual intercourse could result in a 38-week commitment of human gestation and subsequent commitments related to rearing such as breastfeeding. From Trivers' theory of parental investment, several implications follow. The first implication is that women are often but not always the more investing sex. The fact that they are often the more investing sex leads to the second implication that evolution favors females who are more selective of their mates to ensure that intercourse would not result in unnecessary or wasteful costs. The third implication is that because women invest more and are essential for the reproductive success of their offspring, they are a valuable resource for men; as a result, males often compete for sexual access to females.

Males as the more investing sex

For many species the only type of male investment received is that of sex cells. In those terms, the female investment greatly exceeds that of male investment as previously mentioned. However, there are other ways in which males invest in their offspring. For example, the male can find food as in the example of balloon flies.^[26] He may find a safe environment for the female to feed or lay her eggs as exemplified in many birds.^[27][28]

He may also protect the young and provide them with opportunities to learn as young, as is the case with many wolves. Overall, the main role that males overtake is that of protection of the female and their young. That often can decrease the discrepancy of investment caused by the initial investment of sex cells. There are some species such as the Mormon cricket, pipefish seahorse and Panamanian poison arrow frog males invest more. Among the species where the male invests more, the male is also the pickier sex, placing higher demands on their selected female. For example, the female that they often choose usually contain 60% more eggs than rejected females.

International politics

Parental investment theory is not only used to explain evolutionary phenomena and human behavior but describes recurrences in international politics as well. Specifically, parental investment is referred to when describing competitive behaviors between states and determining aggressive nature of foreign policies. The parental investment hypothesis states that the size of coalitions and the physical strengths of its male members determines whether its activities with its foreign neighbors are aggressive or amiable. According to Trivers, men have had relatively low parental investments, and were therefore forced into fiercer competitive situations over limited reproductive resources. Sexual selection naturally took place and men have evolved to address its unique reproductive problems. Among other adaptations, men's psychology has also developed to directly aid men in such intra-sexual competition.

One essential psychological developments involved decision-making of whether to take flight or actively engage in warfare with another rivalry group. The two main factors that men referred to in such situations were (1) whether the coalition they are a part of is larger than its opposition and (2) whether the men in their coalition have greater physical strength than the other. The male psychology conveyed in the ancient past has been passed on to modern times causing men to partly think and behave as they have during ancestral wars. According to this theory, leaders of international politics were not an exception. For example, the United States expected to win the Vietnam War due to its greater military capacity when compared to its enemies. Yet victory, according to the traditional rule of greater coalition size, did not come about because the U.S. did not take enough consideration to other factors, such as the perseverance of the local population.

The parental investment hypothesis contends that male physical strength of a coalition still determines the aggressiveness of modern conflicts between states. While this idea may seem unreasonable upon considering that male physical strength is one of the least determining aspects of today's warfare, human psychology has nevertheless evolved to operate on this basis. Moreover, although it may seem that mate seeking motivation is no longer a determinant, in modern wars sexuality, such as rape, is undeniably evident in conflicts even to this day.

Pair of crested auklets

Sexual selection

Main article: Sexual selection

In many species, males can produce a larger number of offspring over the course of their lives by minimizing parental investment in favor of investing time impregnating any reproductive-age female who is fertile. In contrast, a female can have a much smaller number of offspring during her reproductive life, partly due to higher obligate parental investment. Females will be more selective ("choosy") of mates than males will be, choosing males with good fitness (e.g., genes, high status, resources, etc.), so as to help offset any lack of direct parental investment from the male, and therefore increase reproductive success. Robert Trivers' theory of parental investment predicts that the sex making the largest investment in lactation, nurturing, and protecting offspring will be more discriminating in mating; and that the sex that invests less in offspring will compete via intrasexual selection for access to the higher-investing sex (see Bateman's principle).

In species where both sexes invest highly in parental care, mutual choosiness is expected to arise. An example of this is seen in crested auklets, where parents share equal responsibility in incubating their single egg and raising the chick. In crested auklets, both sexes are ornamented.

Parental investment in humans

Humans have evolved increasing levels of parental investment, both biologically and behaviorally. The fetus requires high investment from the mother, and the altricial newborn requires high investment from a community. Species whose newborn young are unable to move on their own and require parental care have a high degree of altriciality. Human children are born unable to care for themselves and require additional parental investment post-birth in order to survive.

Maternal investment

Trivers (1972) hypothesized that greater biologically obligated investment will predict greater voluntary investment. Mothers invest an impressive amount in their children before they are even born. The time and nutrients required to develop the fetus, and the risks associated with both giving these nutrients and undergoing childbirth, are a sizable investment. To ensure that this investment is not for nothing, mothers are likely to invest in their children after they are born, to be sure that they survive and are successful. Relative to most other species, human mothers give more resources to their offspring at a higher risk to their own health, even before the child is born. This is associated with the evolution of a slower life history, in which fewer, larger offspring are born after longer intervals, requiring increased parental investment.

The placenta attaches to the uterine wall, and the umbilical cord connects it to the fetus.

The developing human fetus––and especially the brain––requires nutrients to grow. In the later weeks of gestation, the fetus requires increasing nutrients as the growth of the brain increases. Rodents and primates have the most invasive placenta phenotype, the hemochorial placenta, in which the chorion erodes the uterine epithelium and has direct contact with maternal blood. The other placental phenotypes are separated from the maternal bloodstream by at least one layer of tissue. The more invasive placenta allows for a more efficient transfer of nutrients between the mother and fetus, but it comes with risks as well. The fetus is able to release hormones directly into the mother's bloodstream to “demand” increased resources. This can result in health problems for the mother, such as pre-eclampsia. During childbirth, the detachment of the placental chorion can cause excessive bleeding.

The obstetrical dilemma also makes birth more difficult and results in increased maternal investment. Humans have evolved both bipedalism and large brain size. The evolution of bipedalism altered the shape of the pelvis, and shrunk the birth canal at the same time brains were evolving to be larger. The decreasing birth canal size meant that babies are born earlier in development, when they have smaller brains. Humans give birth to babies with brains 25% developed, while other primates give birth to offspring with brains 45-50% developed. A second possible explanation for the early birth in humans is the energy required to grow and sustain a larger brain. Supporting a larger brain gestationally requires energy the mother may be unable to invest.

The obstetrical dilemma makes birth challenging, and a distinguishing trait of humans is the need for assistance during childbirth. The altered shape of the bipedal pelvis requires that babies leave the birth canal facing away from the mother, contrary to all other primate species. This makes it more difficult for the mother to clear the baby's breathing passageways, to make sure the umbilical cord is not wrapped around the neck, and to pull the baby free without bending its body the wrong way.

The human need to have a birth attendant also requires sociality. In order to guarantee the presence of a birth attendant, humans must aggregate in groups. It has been controversially claimed that humans have eusociality, like ants and bees, in which there is relatively high parental investment, cooperative care of young, and division of labor. It is unclear which evolved first; sociality, bipedalism, or birth attendance. Bonobos, our closest living relatives alongside chimpanzees, have high female sociality and births among bonobos are also social events. Sociality may have been a prerequisite for birth attendance, and bipedalism and birth attendance could have evolved as long as five million years ago.

A baby, mother, grandmother, and great-grandmother. In humans, grandparents often help to raise a child.

As female primates age, their ability to reproduce decreases. The grandmother hypothesis describes the evolution of menopause, which may or may not be unique to humans among primates. As women age, the costs of investing in additional reproduction increase and the benefits decrease. At menopause, it is more beneficial to stop reproduction and begin investing in grandchildren. Grandmothers are certain of their genetic relation to their grandchildren, especially the children of their daughters, because maternal certainty of their own children is high, and their daughters are certain of their maternity to their children as well. It has also been theorized that grandmothers preferentially invest in the daughters of their daughters because X chromosomes carry more DNA and their granddaughters are most closely related to them.

Paternal investment

See also: Paternal care

As altriciality increased, investment from individuals other than the mother became more necessary. High sociality meant that female relatives were present to help the mother, but paternal investment increased as well. Paternal investment increases as it becomes more difficult to have additional children, and as the effects of investment on offspring fitness increase.

Men are more likely than women to give no parental investment to their children, and the children of low-investing fathers are more likely to give less parental investment to their own children. Father absence is a risk factor for both early sexual activity and teenage pregnancy. Father absence raises children's stress levels, which are linked to earlier onset of sexual activity and increased short-term mating orientation. Daughters of absent fathers are more likely to seek short-term partners, and one theory explains this as a preference for outside (non-partner) social support because of the perceived uncertain future and uncertain availability of committing partners in a high-stress environment.

Investment as predictor of mating strategies

Chance of fertilization by menstrual cycle day relative to ovulation, with data from two different studies

Concealed ovulation

Main article: Concealed ovulation

Women can only get pregnant while ovulating. Human ovulation is concealed, or not signaled externally. Concealed ovulation decreases paternity certainty because men are unsure when women ovulate. The evolution of concealed ovulation has been theorized to be a result of altriciality and increased need for paternal investment—if men are unsure of the time of ovulation, the best way to successfully reproduce would be to repeatedly mate with a woman throughout her cycle, which requires pair bonding, which in turn increases paternal investment.

Mating orientations

See also: Human mating strategies

Sociosexuality was first described by Alfred Kinsey as a willingness to engage in casual and uncommitted sexual relationships. Sociosexual orientation describes sociosexuality on a scale from unrestricted to restricted. Individuals with an unrestricted sociosexual orientation have higher openness to sex in less committed relationships, and individuals with a restricted sociosexual orientation have lower openness to casual sexual relationships. However, today it is acknowledged that sociosexuality does not in reality exist on a one-dimensional scale. Individuals who are less open to casual relationships are not always seeking committed relationships, and individuals who are less interested in committed relationships are not always interested in casual relationships. Short- and long-term mating orientations are the modern descriptors of openness to uncommitted and committed relationships, respectively.

Parental investment theory, as proposed by Trivers, argues that the sex with higher obligatory investment will be more selective in choosing sex partners, and the sex with lower obligatory investment will be less selective and more interested in "casual" mating opportunities. The more investing sex cannot reproduce as frequently, causing the less investing sex to compete for mating opportunities. In humans, women have higher obligatory investment (pregnancy and childbirth), than men (sperm production). Women are more likely to have higher long-term mating orientations, and men are more likely to have higher short-term mating orientations.

Short- and long-term mating orientations influence women's preferences in men. Studies have found that women put great emphasis on career-orientation, ambition and devotion only when considering a long-term partner. When marriage is not involved, women put greater emphasis on physical attractiveness. Generally, women prefer men who are likely to perform high parental investment and have good genes. Women prefer men with good financial status, who are more committed, who are more athletic, and who are healthier.

Some inaccurate theories have been inspired by parental investment theory. The "structural powerlessness hypothesis" proposes that women strive to find mates with access to high levels of resources because as women, they are excluded from these resources directly. However, this hypothesis has been disproved by studies which found that financially successful women place an even greater importance on financial status, social status, and possession of professional degrees.

Polygyny

Decreased polygyny is associated with increased paternal investment.

The demographic transition

See also: Demographic transition

The demographic transition describes the modern decrease in both birth and death rates. From a Darwinian perspective, it does not make sense that families with more resources are having fewer children. One explanation for the demographic transition is the increased parental investment required to raise children who will be able to maintain the same level of resources as their parents.

Paternal care

From Wikipedia, the free encyclopedia

https://en.wikipedia.org/wiki/Paternal_care

In biology, paternal care is parental investment provided by a male to his own offspring. It is a complex social behaviour in vertebrates associated with animal mating systems, life history traits, and ecology. Paternal care may be provided in concert with the mother (biparental care) or, more rarely, by the male alone (so called exclusive paternal care).

The provision of care, by either males or females, is presumed to increase growth rates, quality, and/or survival of young, and hence ultimately increase the inclusive fitness of parents. In a variety of vertebrate species (e.g., about 80% of birds and about 6% of mammals), both males and females invest heavily in their offspring. Many of these biparental species are socially monogamous, so individuals remain with their mate for at least one breeding season.

Exclusive paternal care has evolved multiple times in a variety of organisms, including invertebrates, fishes, and amphibians.

Mammals

Pack of African wild dogs (Lycaon pictus) resting. A mammal in which males remain as care helpers.

Male mammals employ different behaviors to enhance their reproductive success (e.g. courtship displays, mate choice). However, the benefits of paternal care have rarely been studied in mammals, largely because only 5-10% of mammals exhibit such care (mostly present in primates, rodents and canids). In those species in which males provide extensive care for their offspring, indirect evidence suggests that its costs can be substantial. For example, mammalian fathers that care for their young may undergo changes in body mass and an increase in production of a number of costly hormones (e.g. androgens, glucocorticoids, leptin). Nonetheless, there is evidence that suggest that across all mammals, when males carry and groom their offspring their female partner fecundity increases, and if males provision the females, their litter size tend to be larger.

Humans

Main article: Father

Human cultures and societies vary widely in the expression of paternal care. Some cultures recognize paternal care via celebration of Father's Day. Human paternal care is a derived characteristic (evolved in humans or our recent ancestors) and one of the defining characteristics of Homo sapiens. Different aspects of human paternal care (direct, indirect, fostering social or moral development) may have evolved at different points in our history, and together they form a unique suite of behaviors as compared with the great apes. One study of humans has found evidence suggesting a possible evolutionary trade-off between mating success and parenting involvement; specifically, fathers with smaller testes tend to be more involved in care of their children.

Research on the effects of paternal care on human happiness have yielded conflicting results. However, one recent study concluded that fathers generally report higher levels of happiness, positive emotion, and meaning in life as compared with non-fathers.

According to the United States Census Bureau, approximately one third of children in the U.S. grow up without their biological father in their home. Numerous studies have documented negative consequences of being raised in a home that lacks a father, including increased likelihood of living in poverty, having behavioral problems, committing crimes, spending time in prison, abusing drugs or alcohol, becoming obese, and dropping out of school.

Non-human primates

In non-human primates, paternal investment is often dependent on the type of mating system exhibited by each species. Mating systems influence paternity certainty and the likelihood that a male is providing care towards his own biological offspring. Paternal certainty is high in monogamous pair-bonded species and males are less likely to be at risk for caring for unrelated offspring and not contributing to their own fitness. In contrast, polygamous primate societies create paternity uncertainty and males are more at risk of providing care for unrelated offspring and compromising their own fitness. Paternal care by male non-human primates motivated by biological paternity utilize past mating history and phenotypic matching in order to recognize their own offspring. Comparing male care efforts exhibited by the same species can provide insight on the significant relationship between paternity certainty and the amount of paternal care exhibited by a male. For example, Siamangs (Symphalangus syndactylus) utilize both polyandrous and monogamous mating systems but, it was found that monogamous males are more likely to carry infants and contribute to parental duties compared to those in promiscuous mating systems. Studies in Primatology have used primate mating systems and social organization to help theorize the evolutionary significance of paternal care in Primates.

Strepsirrhines

Ring tailed Lemur

Strepsirrhini is a suborder of the order Primates and includes lemurs, lorises, and bush babies. In this sub-order, males exhibit the lowest levels of paternal care for infants among primates. Examples of observed male care in this group include playing, grooming, and occasionally transporting infants. Males have also been observed interacting with infants while mothers park them and temporarily leave in order to feed. When female strepsirrhines park or nest their infants in nearby trees, males frequently use this as an opportunity to play with the unattended infants. In this suborder, male care and affection is directed toward multiple infants including non-biological offspring, and young strepsirrhines can be found interacting with various males. Paternal care does not influence infant growth rates or shorten inter-birth intervals of mothers as it can in haplorrhines. Strepsirrhini males exhibit the lowest intensity of care towards infants in non-human primates.

Strepsirrhines are constrained by their life history traits and reproductive rates are not flexible within this group of primates. This group of primates are programmed to give birth when food is abundant resulting in strict seasonal breeding periods. Shortening inter-birth intervals, which is theorized to be a possible outcome of increased male care, is not beneficial for Strepsirrhine mothers and can decrease infant survival. Studies also show that paternity can be highly skewed in Strepsirrhines, with only one or few male members being the only biological father within a single group. Instead of relying on a singular paternal figure, female mothers in this group rely on alloparenting from other group members. Infant parking and strict reproductive schedules are more beneficial for successful infant development in Strepsirrhines.

Haplorrhines

Chimpanzee infant

Haplorhini, a sub-order of the order Primate, includes tarsiers, New World Monkeys, Old World monkeys, apes, and humans. Haplorrhini is broken into two sister groups which are commonly distinguished by the characteristic of the primate nose: Catarrhini (narrow turned down nose) and Platyrrhini (flat nose). Paternal care is highly variable between the two sister groups and the species within them.

Catarrhines

Catarrhini is composed of Old World Monkeys (Cercopithecidae) and apes (Hylobatidae and Hominoidea). These primates are geographically located in Africa, Asia, and Madagascar.

Cercopithecines, the largest primate family, include primates species such as baboons, macaques, colobus, and vervet monkeys.

Apes consist of species of gibbons, siamangs, bonobos, chimpanzees, gorillas, orangutans and humans.

Catarrhines (non-human) are often organized into a multimale-multifemale social systems and utilize polygamous mating systems which results in paternity uncertainty. It is predicted that males in promiscuous mating systems do not engage in infant care due to the high costs of caring for an infant and missing opportunities to mate with receptive females. Male care in this group of primates is often portrayed through actions such as grooming, carrying, tolerance of the infant, as well as protection against agonistic interactions and infanticide. High ranking males can also provide access to food for developing infants. Direct care such as grooming and playing is not as common compared to male intervention on behalf of the infant when it is being harassed by conspecifics.

Baboon and her infant

In Cercopiths, male involvement in the infant's interactions with others is common in many species of baboons but between species paternal care is not always biased towards biological offspring. Male Savannah baboons (Papio cynocephalus) direct care towards their own biological offspring. Males in this species are more likely to intervene and protect infants from harassment against other group members when the infant is predicted to be their own. Studies have shown that male Savannah baboons selectively choose to remain in closer proximity to their own offspring and engage in long-term investment beyond early infancy, when the infant is at greatest risk for infanticide. Infants receiving paternal investment in Savannah baboons have shown enhanced fitness and accelerated maturation through males creating a safe zone for infants to exist in. Similarly to Savannah Baboons, Yellow baboon (Papio cynocephalus) males provide elevated care for their own offspring. Long-term care and investment beyond early infancy is better linked to paternity in this species and affecting infant growth and development. Male baboons also direct care towards unrelated offspring based on male affiliations with female mothers. Baboon males and females within a social group often exhibit “friendships” with females which begin during birth of her infant and has been observed to end abruptly if the infant dies. Males establish associations with females in which they have previously mated resulting in affiliative behaviour and protection towards her offspring. Relationships created by male and female members are significant for infant survival in Chacma baboons (Papio ursinus) because the risk of infanticide in early infancy is higher in this species. Paternal care in the form of protection for the infant is therefore more beneficial than long term investment in Chacma baboons and is believed to be directed towards both biological and non-biological infants in the group.

Rhesus Macaque

Similarly to baboons, paternal roles and the underlying mechanisms as to why paternal care evolved vary within macaque species. In Sulawesi crested macaques (Macaca nigra) both male rank and the relationship to the mother predicted male care towards an infant instead of true biological paternity. In both Sulawesi and Barbary macaques (Macaca sylvanus) males adopted a “care-then-mate” strategy, in which care is provided to infants regardless of paternity in order for the male to increase future mating opportunities with the mother. In both species, it was observed that male macaques are more likely to initiate care towards and positively interact with the infant in the presence of the mother. In Assamese macaques (Macaca assamensis) biological paternity was the most significant predictor of male affiliations with infants and therefore males biased care towards infants presumed to be their own. Observers found that Assamese males were more likely to engage and provide care for infants in the absence of their mothers reducing the likelihood that care provided to infants will impress the mother and secure access to mating possibilities. In Rhesus macaques, male's providing protection and greater access to food resulted in higher weight gain for both male and female infants. This had a positive effect on infant survival and was significant in the first year of infancy when the risk of infanticide is the highest.

Chimpanzees (Pan troglodytes) are organized into fission-fusion social groups and provide an example of a polygamous mating society. Male chimpanzees often engage with infants in the form of grooming, playing, and providing protection towards other group members. In both Western and Eastern chimpanzees it was found that males were more likely to engage with their own biological offspring meaning that male care is directed by paternity in this species. In both chimpanzee and bonobo social groups, high ranking alpha males sire approximately half of the offspring within their social group. More research needs to be done addressing how reproductive skew affects paternal care and infant-male relationships in non-human primates including chimpanzees and bonobos.

Platyrrhines

Titi Monkey

Platyrrhini is a sub-order of the order Primate and are commonly referred to as the New World Monkeys. These primates occupy Central and South America, and Mexico. This group is broken into five families, range in body size, and include species such as spider monkeys, capuchins, and howler monkeys.

Among primate species, the highest levels of male care found in New World monkeys are observed in Owl monkeys (Aotus azarai ) and Titi monkeys (Callicebus caligatus). In both of these species, males and females are monogamous, pair-bonded, and exhibit bi-parental care for their offspring. The social group in both these species consists of female and male parents along with their offspring. Males in these species serve as the primary caregivers and play a major role in infant survival.

Male Titi monkeys are more involved than the mother in all aspects of male care except nursing, and engage in more social activities such as grooming, food sharing, play, and transportation of the infant. The bond between an infant and its father is established right after birth and maintained into adolescence making the father the infant's predominant attachment figure. Similarly, the male Owl monkey acts as the main caregiver and is crucial to the survival of his offspring. If a female gives birth to twins, the male is still responsible for transporting both the infants. In the absence of a father, infant mortality increases in both these species and it is unlikely that the infant will survive. One study found that the replacement of a male enacting as the role of the father resulted in higher mortality during infancy emphasizing the importance of the social bond created between father and offspring at birth.

White-faced Capuchin

In White‐faced Capuchins (Cebus capucinus) one study found that parental care was exhibited in the form of playful behaviour, proximity to, inspection of, and collecting discarded food items from infants as determined by male rank and dominance status rather than biological relatedness to the infant. Scientists believe that future research on kin recognition needs to be done on capuchins to determine if males choose to bias their care as well as in other non-human primates relying on phenotypic matching to distinguish biological offspring.

Evolutionary Perspectives on Paternal Care in Primates

Squirrel monkeys

The Theory of Paternal Investment: Differences in infant care between sexes stems from females investing more time and energy in their offspring than males, while males compete with one another for access to females. Although paternal care is rare among mammalians, males across many primate species still play a paternal role in infant care.

Hypotheses addressing the rise of paternal care in several primate species

The Paternal Care hypothesis: Paternal care and investment will be designated to biological offspring, increasing the infant's chance of survival, and therefore increasing the male's own fitness. This hypothesis requires the on male to use recognition and behavioural cues to distinguish their own offspring from other infants. Paternal uncertainty is high in multimale-multifemale primate groups so males must use these cues to recognize and bias care towards their own offspring. This allows males to provide both short and long-term investment for infants. Primates living in monogamous pairs or single-male groups exhibit high paternity certainty and assist with the Paternal Care hypothesis.

The Mating Effort hypothesis: Males provide care for infants in order to increase mating opportunities with females. This means that males are more likely to engage in affiliative behaviours with the infant in the presence of the mother as a form of male mating effort in order to enhance future reproductive success. This theory is independent of genetics and evolved independent of paternity.

The Maternal Relief hypothesis: Males provide care infants to help reduce reproductive burdens of the female, ultimately resulting shorter inter-birth intervals and more successful offspring. This stems from the male alleviating the female from her parental duties in order to keep her resources from becoming depleted and subsequently allowing her to produce high quality milk for the infant. Similarly to the mating effort hypothesis, the maternal relief hypothesis is independent of genetics and does not require the male to be the biological father to take part in infant care.

Rodents

California mice (Peromyscus californicus) are well known for have intensive and sustained paternal behavior.

Several species of rodents have been studied as models of paternal care, including prairie voles (Microtus ochrogaster), Campbell's dwarf hamster, the Mongolian gerbil, and the African striped mouse. The California mouse (Peromyscus californicus) is a monogamous rodent that exhibits extensive and essential paternal care, and hence has been studied as a model organism for this phenomenon. One study of this species found that fathers had larger hindlimb muscles than did non-breeding males. Quantitative genetic analysis has identified several genomic regions that affect paternal care.

Birds

Main article: Parental care in birds

Fathers contribute equally with mothers to the care of offspring in as many as 90% of bird species, sometimes including incubating the eggs. Most paternal care is associated with biparental care in socially monogamous mating systems (about 81% of species), but in approximately 1% of species, fathers provide all care after eggs are laid. The unusually high incidence of paternal care in birds compared to other vertebrate taxa is often assumed to stem from the extensive resource requirements for production of flight-capable offspring. By contrast, in bats (the other extant flying vertebrate lineage), care of offspring is provided by females (although males may help guard pups in some species). In contrast to the large clutch sizes found in many bird species with biparental care, bats typically produce single offspring, which may be a limitation related to lack of male help. It has been suggested, though not without controversy, that paternal care is the ancestral form of parental care in birds.

Amphibians

Paternal care occurs in a number of species of anuran amphibians, including glass frogs.

Fish

According to the Encyclopedia of Fish Physiology: From Genome to Environment:

About 30% of the 500 known fish families show some form of parental care, and most often (78% of the time) care is provided by only one parent (usually the male). Male care (50%) is much more common than female care (30%) with biparental care accounting for about 20%, although a more recent comparative analysis suggests that male care may be more common (84%).

There are three common theoretical explanations for the high levels of paternal care in fish, with the third one currently favoured. First, external fertilization protects against paternity loss; however, sneaker tactics and strong sperm competition have evolved many times. Second, the earlier release of eggs than sperm gives females an opportunity to flee; however, in many paternal care species, eggs and sperm are released simultaneously. Third, if a male is already protecting a valuable spawning territory in order to attract females, defending young adds minimal parental investment, giving males a lower relative cost of parental care.

One well-known example of paternal care is in seahorses, where males brood the eggs in a brood pouch until they are ready to hatch.

Males from the Centrarchidae (sunfish) family exhibit paternal parental care of their eggs and fry through a variety of behaviors such as nest guarding and nest fanning (aerating eggs).

In jawfish, the female lays the eggs and the male then takes them in his mouth. A male can have up to 400 eggs in his mouth at one time. The male can't feed while he hosts the young, but as the young get older, they spend more time out of the mouth. This is sometimes termed mouthbrooding.

During the breeding season, male three-spined sticklebacks defend nesting territories. Males attract females to spawn in their nests and defend their breeding territory from intruders and predators. After spawning, the female leaves the male's territory and the male is solely responsible for the care of the eggs. During the ~6-day incubation period, the male 'fans' (oxygenates) the eggs, removes rotten eggs and debris, and defends the territory. Even after embryos hatch, father sticklebacks continue to tend their newly hatched offspring for ~7 days, chasing and retrieving fry that stray from the nest and spitting them back into the nest.

Arthropods

Paternal care is rare in arthropods, but occurs in some species, including the giant water bug and the arachnid Iporangaia pustulosa, a harvestman. In several species of crustaceans, males provide care of offspring by building and defending burrows or other nest sites. Exclusive paternal care, where males provide the sole investment after egg-laying, is the rarest form, and is known in only 13 taxa: giant water bugs, sea spiders, two genera of leaf-footed bugs, two genera of assassin bugs, three genera of phlaeothripid thrips, three genera of harvestmen, and in millipedes of the family Andrognathidae.

Theoretical models of the evolution of paternal care

Mathematical models related to the prisoner's dilemma suggest that when female reproductive costs are higher than male reproductive costs, males cooperate with females even when they do not reciprocate. In this view, paternal care is an evolutionary achievement that compensates for the higher energy demands that reproduction typically involves for mothers.

Other models suggest that basic life-history differences between males and females are adequate to explain the evolutionary origins of maternal, paternal, and bi-parental care. Specifically, paternal care is more likely if male adult mortality is high, and maternal care is more likely to evolve if female adult mortality is high. Basic life-history differences between the sexes can also cause evolutionary transitions among different sex-specific patterns of parental care.

Consequences for offspring survival and development

Care by fathers can have important consequences for survival and development of offspring in both humans and other species. Mechanisms underlying such effects may include protecting offspring from predators or environmental extremes (e.g., heat or cold), feeding them or, in some species, direct teaching of skills. Moreover, some studies indicate a potential epigenetic germline inheritance of paternal effects.

The effects of paternal care on offspring can be studied in various ways. One way is to compare species that vary in the degree of paternal care. For example, an extended duration of paternal care occurs in the gentoo penguin, as compared with other Pygoscelis species. It was found that their fledging period, the time between a chick's first trip to sea and its absolute independence from the group, was longer than other penguins of the same genus. The authors hypothesized that this was because it allowed chicks to better develop their foraging skills before becoming completely independent from their parents. By doing so, a chick may have a higher chance of survival and increase the population's overall fitness.

Proximate mechanisms

The proximate mechanisms of paternal care are not well understood for any organism. In vertebrates, at the level of hormonal control, vasopressin apparently underlies the neurochemical basis of paternal care; prolactin and testosterone may also be involved. As with other behaviors that affect Darwinian fitness, reward pathways in the brain may reinforce the expression of paternal care and may be involved in the formation of attachment bonds.

The mechanisms that underlie the onset of parental behaviors in female mammals have been characterized in a variety of species. In mammals, females undergo endocrine changes during gestation and lactation that "prime" mothers to respond maternally towards their offspring.

Paternal males do not undergo these same hormonal changes and so the proximate causes of the onset of parental behaviors must differ from those in females. There is little consensus regarding the processes by which mammalian males begin to express parental behaviors. In humans, evidence ties oxytocin to sensitive care-giving in both women and men, and with affectionate infant contact in women and stimulatory infant contact in men. In contrast, testosterone decreases in men who become involved fathers and testosterone may interfere with aspects of paternal care.

Placentophagia (the behavior of ingesting the afterbirth after parturition) has been proposed to have physiological consequences that could facilitate a male's responsiveness to offspring. Non-genomic transmission of paternal behavior from fathers to their sons has been reported to occur in laboratory studies of the biparental California mouse, but whether this involves (epigenetic) modifications or other mechanisms is not yet known.

Challenge hypothesis

From Wikipedia, the free encyclopedia
https://en.wikipedia.org/wiki/Challenge_hypothesis

The challenge hypothesis outlines the dynamic relationship between testosterone and aggression in mating contexts. It proposes that testosterone promotes aggression when it would be beneficial for reproduction, such as mate guarding, or strategies designed to prevent the encroachment of intrasexual rivals. The positive correlation between reproductive aggression and testosterone levels is seen to be strongest during times of social instability. The challenge hypothesis predicts that seasonal patterns in testosterone levels are a function of mating system (monogamy versus polygyny), paternal care, and male-male aggression in seasonal breeders.

The pattern between testosterone and aggression was first observed in seasonally breeding birds, where testosterone levels rise modestly with the onset of the breeding season to support basic reproductive functions. However, during periods of heightened male aggression, testosterone levels increase further to a maximum physiological level. This additional boost in testosterone appears to facilitate male-male aggression, particularly during territory formation and mate guarding, and is also characterized by a lack of paternal care. The challenge hypothesis has come to explain patterns of testosterone production as predictive of aggression across more than 60 species.

Patterns of testosterone

The challenge hypothesis presents a three-level model at which testosterone may be present in circulation. The first level (Level A) represents the baseline level of testosterone during the non-breeding season. Level A is presumed to maintain feedback regulation of both GnRH and gonadotropin release, which are key factors in testosterone production. The next level (Level B) is a regulated, seasonal breeding baseline. This level is sufficient for the expression of reproductive behaviors in seasonal breeders and the development of some secondary sex characteristics. Level B is induced by environmental cues, such as length of day. The highest level (Level C) represents the physiological testosterone maximum and is reached through social stimulation, such as male-male aggression. The challenge hypothesis proposes that social stimulation which leads to this rise in testosterone above breeding baseline serves to increase the frequency and intensity of aggression in males, particularly for competing with other males or interacting with sexually receptive females.

In birds

It is thought that testosterone plays an integral part of the territorial behavior within bird species, in particular the fluctuation of testosterone mitigated by luteinizing hormone (LH) during different seasons. Generally, mating behavior is demonstrated in the spring and accordingly, male birds show a sharp increase in LH as well as testosterone during this time. This acute rise in LH and testosterone can be attributed to the increased need for aggressive behaviors. The first need for aggressive behavior comes from the drive to establish territory. This typically occurs within the first few weeks of mating season. The second need for aggression occurs after the first clutch of eggs have been laid. The male not only needs to guard the eggs, but also to guard his sexually receptive mate from other potential suitors. Thus, the male adopts an “alpha male status” when acquiring territory as well as during the egg laying period. This alpha male status, as mentioned before, comes from the significant increase of testosterone that occurs during the mating season. Further evidence of LH and testosterone mitigating aggression in bird species comes from studies on bird species such as the song sparrow and the European blackbird who build highly accessible refuges, known as open cup nests.

Song sparrow

Because open cup nests can essentially be built anywhere, there is little competition when it comes to nest building sites. Accordingly, both the song sparrow and the European blackbird do not show an increase in luteinizing hormone or testosterone during territory acquisition . However, not all species of birds show increased levels of testosterone and LH during aggressive behavior. In a landmark study, it was found that male western screech owls, when exposed to another male during the non-mating season showed aggressive behavior without the increase in LH and testosterone. However, when the owls were put in a situation that warranted aggressive behavior during the mating season, there was a large spike in LH and testosterone during the aggressive act. This suggests that the mechanisms of aggressive behavior during the mating and non-mating seasons are independent of each other or perhaps the increase in testosterone somehow increases the aggressive response during the mating season. Estradiol (E2), a type of non gonadal estrogen, seems to play a key role in regulating aggressive behavior during the non-mating season in several species of birds. As previously noted, many bird species during the non-mating season have low testosterone levels yet still manage to display aggression. As a primary example, when the Washington State song sparrow, a bird which shows fairly high levels of aggression during non-mating season despite low testosterone, is exposed to fadrozole, an aromatase inhibitor, the levels of aggression are greatly decreased. When the E2 was replaced, the aggressive behaviors reestablished themselves thus confirming that E2 governs aggressive behavior during the non-mating season. It is unknown however if this is just specific to birds, or if this extends to other animal species.

These examples all culminate in a challenge hypothesis model which focuses on the role of testosterone on aggression in the breeding season. The challenge hypothesis most likely cannot be applied to the non-breeding season since, as mentioned above, there is most likely a mechanism independent of testosterone governing aggression in the non-mating season. A sigmoidal relationship between testosterone plasma levels and male-male aggression is observed under the challenge hypothesis when the birds’ testosterone levels were above seasonal breeding testosterone baseline levels. If birds remained at the seasonal breeding baseline levels during the breeding season, then there is not a significant difference observed in male-male aggression. In addition, there is a negative, sigmoidal relationship between testosterone levels in the birds and the amount of parental care provided when parents are above the seasonal breeding testosterone baseline levels. As such, the relationship between testosterone plasma levels and male-male aggression is context-specific to the species. Figure 2 and 3 describe the relationships observed of many single- or double-brooded bird species, from male western gulls to male turkeys.

In other animals

The challenge hypothesis has been used to describe the testosterone levels in other species to certain social stimuli. The challenge hypothesis predicts the testosterone influence on aggressive male-male interactions between male northern fence lizards. This reinforces the challenge hypothesis by showing rapid changes in aggressive behaviors of the lizards do not correlate with testosterone concentrations. Yet, over the mating season, the intensity of the behavior and the levels of testosterone levels yielded a positive correlation. Research has also shown the challenge hypothesis applies to specific monogamous fish species, with a greater correlation in species with stronger pair bonding.

In addition, the challenge hypothesis has been adapted to primate species. In 2004, Martin N. Muller and Richard W. Wrangham applied a modified challenge hypothesis to chimpanzees. Similar to the original hypothesis, they predicted that there would be increased male-male aggressive interaction when a receptive and fertile female chimpanzee was present. Muller and Wrangham also correctly predicted the testosterone levels of more dominant chimpanzees to be higher as compared to lower status chimpanzees. Therefore, chimpanzees significantly increased both testosterone levels and aggressive male-male interactions when receptive and fertile females presented sexual swellings. This study also highlighted how male testosterone and aggression levels rise only when males are in the presence of parous females. This is because nulliparous females are less attractive to males, and they are not guarded, meaning there is little competition. This evidence suggests that the increase in testosterone is related to only aggression – not sexual activity – as male chimpanzees mate equally with both parous and nulliparous females. Currently, no research has specified a relationship between the modified challenge hypothesis and human behavior, yet, many testosterone/human behavior studies support the modified hypothesis applying to human primates.

Cornerstones

Mating effort versus parenting effort

A fundamental feature of male life history is the tradeoff between the energy devoted to male-male competition and mate attraction (mating effort) versus that allocated to raising offspring (parenting effort). There is a trade off because decreased paternal effort caused by increased testosterone dramatically decreases reproductive success, due to decreased parental care and protection for the offspring. Therefore, to maximise reproductive success, the optimal balance between the two must be found. The challenge hypothesis proposes testosterone as the key physiological mechanism underlying this tradeoff. When the opportunity to reproduce arises—namely, the species enters the breeding season or females enter estrus—males should exhibit a rise in testosterone levels to facilitate sexual behavior. This will be characterized by increased mating effort and decreased parenting effort, as investment in the former may be incompatible with parental care due to insufficient time and energy to engage in all of these facets of reproductive effort.

Research on nonhuman species has found that testosterone levels are positively associated with mating effort and negatively related to parenting effort. Moreover, experimental manipulations have revealed a causal role of testosterone, such that elevations in testosterone result in increased mating effort and decreased parenting effort.

Paternal care

The challenge hypothesis makes different predictions regarding testosterone secretion for species in which males exhibit paternal care versus those in which males do not. When aggressive interactions among males arise in species that exhibit paternal care, testosterone levels are expected to be elevated. Males are predicted to exhibit an increase in testosterone to Level C (physiological maximum), but only during periods of territory establishment, male-male challenges, or when females are fertile so that paternal care is not compromised. When aggression is minimal, specifically during parenting, testosterone levels should decrease to Level B (breeding baseline). Level B represents the minimal levels of testosterone required for the expression of reproductive behaviors, and is not expected to drastically interfere with parenting behavior.

In species where males exhibit minimal to no paternal care, testosterone levels are hypothesized to be at Level C throughout the breeding season because of intense and continued interactions between males and the availability of receptive females. In polygynous species, where a single male tends to breed with more than one female, males generally do not exhibit a heightened endocrine response to challenges, because their testosterone levels are already close to physiological maximum throughout the breeding season. Experimental support for the relationship between heightened testosterone and polygyny was found, such that if testosterone was implanted into normally monogamous male birds (i.e., testosterone levels were manipulated to reach Level C) then these males became polygynous.

Mating Effort versus Maintenance

There is a broader trade-off to consider when it comes to the challenge hypothesis: maintenance vs reproductive effort. Reproductive effort includes both mating and parental effort. In order to gain the benefits of reproductive effort, individuals have to suffer the costs of testosterone, which can hinder their physiological maintenance. This is a form of life history tradeoff, due to the fact that natural selection favors reproductive success rather than maintenance. Therefore, the ability to find the correct balance between reproductive effort and maintenance would have been positively selected for by natural selection, leading to the physiological and social behaviour we now know as the challenge hypothesis.

One such cost is that increased aggressive activity due to high levels of testosterone is hypothesised to expose males to increased predation, which not only endangers them, but also their offspring. A study on the lizard Sceloporus jarrovi, supported this prediction, as those with induced high levels of testosterone for extended periods of time had a higher mortality rate than those with lower levels of testosterone. Prolonged high levels of testosterone have also been seen to suppress the immune system, with evidence ranging from human natural experiments to male-ring-tailed lemurs. Maintaining high levels of testosterone is energetically expensive, which can hinder reproductive success when a male frequently finds himself in aggressive and physically demanding situations. Due to increased aggression as a result of high testosterone levels, individuals expose themselves to higher injury risk than usual.

Therefore, the costs of maintaining a high testosterone level may outweigh increased reproductive success. A study on male ring-tailed lemurs (Lemur catta) supports the idea of a compromise between costs and benefits of increased testosterone levels, as increased levels were tightly timed around days of female estrus. This shows that there is an optimum length of time to have high testosterone levels when considering the costs and benefits.

Male-male aggression

It has long been known that testosterone increases aggressive behavior. While castration tends to decrease the frequency of aggression in birds and replacement therapy with testosterone increases aggression, aggression and testosterone are not always directly related. The challenge hypothesis proposes that testosterone is most immediately related to aggression when associated with reproduction, such as mate-guarding. An increase in male-male aggression in the reproductive context as related to testosterone is strongest in situations of social instability, or challenges from another male for a territory or access to mates.

The relationship between aggression and testosterone can be understood in light of the three-level model of testosterone as proposed by the challenge hypothesis. As testosterone reaches Level B, or breeding baseline, there is minimal increase in aggression. As testosterone increases above Level B and approaches Level C, male-male aggression rapidly increases.

Continuous breeders

The challenge hypothesis was established based upon data examining seasonal breeders. There are many species, however, who are continuous breeders—namely, species that breed year-round and whose mating periods are distributed throughout the year (e.g., humans). In continuous breeders, females are sexually receptive during estrus, at which time ovarian follicles are maturing and ovulation can occur. Evidence of ovulation, the phase during which conception is most probable, is advertised to males among many non-human primates via swelling and redness of the genitalia.

Support for the challenge hypothesis has been found in continuous breeders. For example, research on chimpanzees demonstrated that males became more aggressive during periods when females displayed signs of ovulation. Moreover, male chimpanzees engaged in chases and attacks almost 2.5 times more frequently when in groups containing sexually receptive females.

Implications for humans

The predictions of the challenge hypothesis as applied to continuous breeders partially rests upon males' ability to detect when females are sexually receptive. In contrast to females of many animal species who advertise when they are sexually receptive, human females do not exhibit cues but are said to conceal ovulation. While the challenge hypothesis has not been examined in humans, some have proposed that the predictions of the challenge hypothesis may apply.

Several lines of converging evidence in the human literature suggest that this proposition is plausible. For example, testosterone is lower in fathers as compared to non-fathers, and preliminary evidence suggests that men may be able to discern cues of fertility in women. The support for the challenge hypothesis in non-human animals provides a foundation for which to explore the relationship between testosterone and aggression in humans.

The Dual Hormone Hypothesis as an Extension of the Challenge Hypothesis

The challenge hypothesis claims that there is an association between testosterone and aggression in mating contexts, and more broadly status-seeking behaviours. However, findings linking testosterone to status-seeking behaviours, especially in humans, are often inconsistent and leave room for critique. In some cases, testosterone has been seen to positively correlate with status-seeking behaviours such as aggression and competitiveness, however, testosterone has also been found to have weak or even null correlations with the same behaviours. Some scholars blame these inconsistencies on limitations in study methods, but the dual-hormone hypothesis has emerged as a theoretical explanation to some of these inconsistencies.

Dual-Hormone Hypothesis

Stress plays a fundamental role in competition and mating, and therefore, the hormones released in response to stress should be considered as well as testosterone when looking at the challenge hypothesis. Cortisol is produced in the hypothalamic-pituitary-adrenal gland and is released when one is under physical or psychological stress; this is relevant to the challenge hypothesis as testosterone-linked status-seeking interactions are often stressful situations.

According to the dual-hormone hypothesis, the correlation between testosterone levels and aggression/status-seeking behaviour is reliant on corresponding cortisol levels; there is a strong correlation between the two when cortisol levels are low, and a weaker or sometimes reversed correlation when cortisol levels are high. There is supporting evidence for this relationship from a study done on humans, which looked at social status, leadership, and aggression. Cortisol is seen as a moderator of the relationship between testosterone and status-seeking/reproductive aggression in this hypothesis.

However, the dual-hormone hypothesis also has its own flaws, and current evidence appears to only partially support the hypothesis, according to a meta-analytical evaluation in 2019 by Dekkers et al. A proposed reasoning for the occasional weak evidence is that cortisol and testosterone, further interact with social context and individual psychology to regulate status-seeking behaviours. One such context is ‘victory-defeat’, where testosterone and cortisol will interact to increase desire to compete again more after losing than winning, as a method of regaining social status. Individual personality also has an effect on the interaction between cortisol and testosterone, and studies have shown that the cortisol x testosterone interaction was statistically significant for only those with high disagreeableness and high emotional instability.