What oxytocin can tell us about the evolution of human prosociality

Modern humans are characterized by their prosociality, a broad term that encompasses intraspecies empathy, social tolerance, cooperation and altruism. These facets of social cognition have been associated with variations in the oxytocin and vasotocin genes (OT and VT) and their receptors (OTR and VTR).To shed light on the genetic basis of this behaviour, scientists from the University of Barcelona (UB) and Rockefeller University carried out a new study comparing the available genomic sequences of these genes between modern humans, non-human primate species (e.g., chimpanzees, bonobos, and macaques) and, for the first time, archaic humans, using all the available genomes of Neanderthals and Denisovans.

In the study, published in the journal Comprehensive Psychoneuroendocrinology, the researchers identified several sites in which modern humans differed from both archaic humans and non-human primates, and others where both modern and archaic humans differed from non-human primates.

"We used an interdisciplinary approach to understand the evolution of hominid prosociality through the lens of the oxytocin and vasotocin receptors, where we combined evidence from modern and archaic genomics, population genetics, transcriptomics, and behavioural and neuroscientific studies, among other methods. These results can shed light on the genetics underlying possible sociality differences identified between modern humans and archaic humans, as well as the similarities between the modern human and bonobo social behaviour," said first author Constantina Theofanopoulou. This research is part of her doctoral thesis carried out under the co-supervision of Cedric Boeckx, ICREA researcher at the Institute of Complex Systems at the UB (UBICS) and Erich D. Jarvis, professor at Rockefeller University.

Variants unique to modern humans in more than 70% of the population

Considering the evidence on modern human prosociality and on the involvement of the oxytocin and vasotocin genes in social behaviours, the researchers hypothesized that the evolution of these genes might elucidate the genetic basis of the evolution of hominin prosociality. With this aim in mind, the study explored the differences between modern humans, archaic humans and non-human primates in polymorphic heterozygous sites in the human genome -- locations where at least two alternative sequences are found in a population. "Past studies that compared the entire modern human genome with the Neanderthal or the chimpanzee genomes have focused on changes that are fixed or nearly fixed in modern humans. This has led to them identifying sites where, for example, all Neanderthals had Adenine (one of the four nucleotides that with guanine, cytosine and thymine form the DNA) and nearly all modern humans (say, 98%) have Guanine. In this study, we searched for differences on locations where, by definition, not all modern humans share the same nucleotide, namely on polymorphic sites, where for example, 70% of the modern human population has Adenine and 30% Cytosine," adds Theofanopoulou.

The researchers identified five sites in the oxytocin and vasotocin receptors where modern humans are unique in one of their two (or more) variants compared to archaic humans and non-human primates, and which are at the same time found in more than 70% of the modern human population. Next, they conducted functional and frequency analyses to establish whether the variants are relevant. They performed a range of analyses on the five sites and found that some of the variants are highly functional, indicating that they have an effect on the molecular function of the proteins activated by these genes.

The researchers also found that these sites are encountered in genome regions that are active in the brain, particularly in the cingulate gyrus, a brain region involved in social cognition-relevant pathways. Moreover, all these sites have been associated in other studies with a plethora of social behaviours or social deficits, such as autism, attention deficit hyperactivity disorder (ADHD), aggression, and so on.

These findings may help to explain some of the social differences between modern humans and what we presume to know about the social behaviours of Neanderthals and Denisovans. "For example, they might be relevant to the smaller social groups attributed to Neanderthals and Denisovans or to the decreased modern human androgenization. They might also be relevant to a different social structure, i.e., Neanderthals have been linked to a polygynous social structure and a higher level of male-male competition than most contemporary modern human populations," says Constantina Theofanopoulou.

Variants present only in modern and archaic humans

The study also found two sites on the oxytocin receptor under a positive selection in modern and archaic humans: that is to say, modern and archaic humans showed a variant that was not present in any other non-human primate. This means that these sites are found in very high percentages in the modern human population (in this case, more than 85%). These same sites have also been associated with a great many social behaviours or deficits, and one of them was predicted to be a highly functional site in their regulation analyses. "The sites that are unique in both us and archaic humans versus non-human primates can elucidate the genetic underpinnings of the progressive social tolerance needed for the intensive cultural transmission of technological innovations (e.g., fire use) in the evolution of humankind, as well as for the reduced aggression indicated by several markers in early hominid evolution, such as the reduction of male canine size and the accelerated demographic success," adds Theofanopoulou.

Convergent sites with bonobos

Lastly, the researchers found three sites where modern humans and bonobos, a primate species that shows convergence of prosocial behaviours with humans, have the same nucleotide. "The convergent sites in modern humans and bonobos could be insightful for understanding the posited similarities in prosociality, social tolerance and cooperation between us and bonobos, and the differences of both compared to chimpanzees. For example, bonobos outperform chimpanzees on tasks relevant to social causality or theory of mind and are more attentive to the face and eyes, suggestive of higher empathic sensitivity," notes the researcher.

All the sites identified in this study have also been independently associated with disorders that include social deficits, such as autism spectrum disorders (ASD). "Understanding developmental disorders through evolutionary lenses can aid into us achieving what we call an evo-devo (evolutionary and developmental biology) understanding of these disorders. If indeed "ontogeny recapitulates phylogeny," then deciphering our evolutionary trajectory may shed light to new genetic spots for clinical research that might, in turn, lead to earlier disorder diagnosis," highlights Constantina Theofanopoulou.

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People who were children when their parents divorced have less 'love hormone'

 People who were children when their parents were divorced showed lower levels of oxytocin -- the so-called "love hormone" -- when they were adults than those whose parents remained married, according to a study led by Baylor University. That lower level may play a role in having trouble forming attachments when they are grown.

Oxytocin -- secreted in the brain and released during bonding experiences such as delivery of a baby or sexual interaction or nursing, even being hugged by a romantic partner -- has been shown in previous research to be important for social behavior and emotional attachments in early life. The oxytocin system also has been linked to parenting, attachment and anxiety.

The new study, published in the Journal of Comparative Psychology, delves into an area that has not been well researched -- a link between oxytocin, early experience and adult outcomes.

"Since the rates of divorce in our society began to increase, there has been concern about the effects of divorce on the children," said lead author Maria Boccia, Ph.D., professor of child and family studies at Baylor University in the Robbins College of Health and Human Sciences. "Most research has focused on short-term effects, like academic performance, or longer-term outcomes like the impact on relationships. How divorce causes these effects, however, is unknown.

"Oxytocin is a neurohormone that is important in regulating these behaviors and is also sensitive to the impact of stressful life events in early life," she said. "This is a first step towards understanding what mechanisms might be involved."

Previous studies of children whose parents were divorced have found that the experience was associated with mood disorders and substance abuse -- behaviors found to be related to oxytocin, Boccia said. Additionally, such childhood experiences as divorce or death of a parent are associated with depression and anxiety in adolescents and adults, as well as with poorer parenting in adulthood, less parental sensitivity and warmth, overreaction and increased use of punishment.

Researchers in the Baylor study examined the effect of the experience of parental divorce in childhood on later adult oxytocin levels. They also asked participants to complete a set of questionnaires on attachment style and other measures.

"What we found was that oxytocin was substantially lower in people who experienced parental divorce compared to those who did not and correlated with responses on several measures of attachment," Boccia said. "These results suggest that oxytocin levels are adversely affected by parental divorce and may be related to other effects that have been documented in people who experience parental divorce."

Animal studies also suggest that one mechanism contributing to the negative effects of early parental separation may be suppression of oxytocin activity.

For the latest study, researchers recruited 128 individuals ages 18 to 62 at two institutions of higher learning in the Southeast United States. Of those, 27.3% indicated their parents were divorced. The average age for participants when their parents divorced was 9 years.

Upon arriving at the study site, participants were asked to empty their bladders, then given a 16-ounce bottle of water to drink before filling out questionnaires about their parents and peers during childhood, as well as their current social functioning. The questions addressed their parents' style, including affection, protection, indifference, over-control and abuse; and their own levels of confidence, discomfort with closeness, need for approval and their styles of relationships and caregiving.

After participants completed the questionnaires, urine samples were collected, and researchers analyzed oxytocin concentrations. The levels were substantially lower in individuals whose childhood experience included their parents' divorce.

Further analysis showed that those individuals rated their parents as less caring and more indifferent. They also rated their fathers as more abusive. Those who experienced parental divorce during childhood were less confident, more uncomfortable with closeness and less secure in relationships. They rated their own caregiving style as less sensitive and close than did the participants whose parents had not divorced.

"One of the first questions I am asked when presenting this research to other scientists is 'does how old the child is when the divorce occurs matter?' That is the most pressing question that we need to explore," Boccia said.

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Scientists find clue to 'maternal instinct'

Lab mouse and pups

Oxytocin is widely referred to as the love hormone and plays an important role in the regulation of social and maternal behavior. In recent years, the oxytocin system in the brain has received tremendous attention as key to new treatments for many mental health disorders, such as anxiety, autism spectrum disorders and postpartum depression. New research led by a biologist and his students at LSU have discovered a group of cells that are activated by oxytocin in one area of female mouse brains that are not present in the same area in male mouse brains.

"Many researchers have attempted to investigate the difference between the oxytocin system in females versus males, but no one has successfully found conclusive evidence until now. Our discovery was a big surprise," said Ryoichi Teruyama, LSU Department of Biological Sciences associate professor, who led this study published in PLOS ONE.

The oxytocin receptor cells are present in the brain area thought to be involved in the regulation of maternal behavior. Moreover, the expression of oxytocin receptors in these cells are only present when estrogen is also present. These imply that these cells are involved in inducing maternal behavior. In addition, it confirms what many recent human studies have shown: there is a connection between an altered expression of oxytocin receptors and postpartum depression.

Postpartum depression contributes to poor maternal health and has negative effects on a child's development. A number of studies have found that children of depressed mothers are at risk for a wide range of cognitive, emotional, behavioral and medical problems. Therefore, postpartum depression is a major public health concern that has significant adverse effects on both mother and child. About 10 to 20 percent of women experience postpartum depression after childbirth.

This new discovery that occurred at LSU opens doors to potential new treatments and drugs for postpartum depression targeting oxytocin receptor cells.

"I think our discovery could be universal to all mammals that exhibit maternal behavior, including humans," Teruyama said.

Student researchers

Study co-author Ryan LeBlanc from Denham Springs was an undergraduate student researcher at LSU whose work was instrumental to this discovery. However, he had little previous research experience before joining Teruyama's lab.

Teruyama recalled that when LeBlanc first approached him to be his mentor, he asked him about his hobbies. LeBlanc said he liked to build plastic models of battleships.

"I certainly don't know much about battleship plastic models, but anyone who can assemble 500 to 2,000 plastic parts into models must be persistent, focused and exceedingly careful. I accepted him gladly thinking he is going to find something extraordinary, and I was right," Teruyama said.

LeBlanc took on the tedious task of finding and marking the exact location of thousands of oxytocin receptor cells with a red pen. He spent more than a month identifying the cells, which was instrumental to this discovery.

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