High-ranking hyena mothers pass their social networks to their cubs
Using 27 years of detailed data on hyena social interactions, a team led by Penn biologists nailed down a pattern of social network inheritance and its implications for social structure, rank, and survival
IMAGE: USING 27 YEARS OF DETAILED DATA ON HYENA SOCIAL INTERACTIONS, A TEAM LED BY PENN BIOLOGISTS NAILED DOWN A PATTERN OF SOCIAL NETWORK INHERITANCE AND ITS IMPLICATIONS FOR SOCIAL STRUCTURE,... view more
CREDIT: KATE SHAW YOSHIDA
Hyenas are a highly social species, living in groups that can number more than 100. But within their clans, there is order: A specific matrilineal hierarchy governs societies in this species where females are dominant to males.
While researchers have intensively studied the social structure of hyenas and other animals, it's only recently that scientists have begun to investigate how this structure arises. A new study led by Penn biologists, which relies upon 27 years of detailed observations of hyena social behavior collected by researchers at Michigan State University, pulls back the curtain on how social order comes to be.
Their findings show that hyenas inherit their mother's social networks, so their social connections resemble their mother's. However, offspring of higher-ranking individuals more faithfully replicate their mother's interactions, winding up with social networks that more closely resemble their mother's than do offspring of females that rank lower on the clan's social ladder. The team reported their findings in the journal Science.
"We knew that the social structure of hyenas is based in part on one's rank in the agonistic hierarchy, which we know is inherited from mothers" says Erol Akçay, a study coauthor and associate professor in Penn's School of Arts & Sciences. "But what we found, that affiliative, or friendly interactions, are also inherited, hadn't been shown."
"This is a very simple process of social inheritance that we show works very, very well," says Amiyaal Ilany, a senior lecturer at Israel's Bar-Ilan University. "Individuals that were born to higher rank are more accurate in their inheritance, and they have good reason to do so. It fits well with what is already known about inheritance of rank. There are very strict rules about what place you sit in the hierarchy if you are a hyena."
The work builds on a theoretical model of social network inheritance Akçay and Ilany developed in 2016. According to that simple framework, animals establish their networks by "social inheritance," or copying their mother's behaviors. The model fit well with snapshots of real-world social networks from not only hyenas but also three other social species: bottle-nosed dolphins, rock hyrax, and sleepy lizards.
In the new work, the team aimed to refine their model to better understand the intricacies of social inheritance in hyenas. They were fortunate to have a robust dataset collected by Akçay and Ilany's coauthor, zoologist Kay Holekamp of Michigan State University, consisting of 27 years of detailed accounting of a clan's social interactions.
"We realized we could use that dataset to directly test our model, to see if social ties are inherited or not," Akçay says.
Field biologists from Holekamp's research group had meticulously tracked how hyenas in a clan interacted, including who spent time with whom as well as the social rank of each member. To do so, researchers spent months getting to know each member of the clan by sight.
"They are there year-round, every day, identifying individuals by their specific spot patterns and other characteristics," Ilany says.
These observations allowed Akçay, Ilany, and Holekamp to map out hyenas' social networks based on which individuals spent time close together.
"This use of proximity to track social networks isn't possible with humans, as two strangers might randomly get into an elevator together," Ilany says. "But with hyenas, if one individual gets within a few meters of another, that suggests that they have a social connection."
With this picture of each individual's social affiliations in hand, the researchers compared the social networks of mothers to their offspring. "We developed a new metric to measure social inheritance, to track how faithfully an offspring's network reproduces its mother's network," Akçay says.
Hyena cubs stick close to their mothers for the first couple years of life, so the networks of mothers and their offsprings were quite similar to start. However, the researchers noticed that even as the young stopped spending so much time in close proximity to their mothers they still sustained quite similar networks, particularly for female offspring, who generally remain members of the clan for life. "We have data in some cases showing that the network similarity between mothers and offspring, especially female offspring, was still very high after six or so years," says Ilany. "You may not be seeing your mother as often, or she even may have died, but you still have similar friends."
This pattern was especially strong for the higher-ranking mothers, for whom social inheritance was the strongest in the group.
"That is kind of intuitive because things like that happen in human society as well," Akçay says. "It happens so much we take it for granted. We inherit social connections, and there's a lot of social science research that shows that this has a huge influence on people's life trajectory."
Offspring of lower-ranking mothers were less likely to reproduce their mother's social networks, perhaps trying to compensate for their more lowly origins by associating with a greater variety of individuals.
There is no genetic inheritance of rank or close associates in this species, so in Holekamp's opinion one of the most remarkable things about the phenomenon documented here is that the youngsters' relationships with their mothers' close associates are all learned very early in life. One explanation for why inheritance of social networks works better for high- than for low-ranking hyenas may be that low-ranking females tend to go off on their own more often to avoid competition with higher-ranking hyenas, so their cubs have fewer learning opportunities than cubs of high-ranking females.
Mother-offspring pairs with more similar social networks also lived longer, the team found. This effect on survivorship may owe to the fact that offspring who spend more time with their mothers and thus replicate their social networks benefit from the increased care.
Social rank also had an effect on survivorship and reproductive success.
"Rank is super important," says Akçay. "If you're born to a lower-ranked mother, you are less likely to survive and to reproduce."
The researchers note that social network inheritance likely contributes to a group's stability and also has implications for how behaviors are learned and spread through groups.
The study also underscores how factors other than genetics hold sway in key evolutionary outcomes, including reproductive success and overall survival. "A lot of things that are considered by default to be genetically determined may depend on environmental and social processes," says Ilany.
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Erol Akçay is an associate professor of biology in the School of Arts & Sciences at the University of Pennsylvania.
Amiyaal Ilany is a senior lecturer at the Mina and Everard Goodman Faculty of Life Sciences at Bar-Ilan University and completed a postdoctoral fellowship working with Akçay at Penn.
Kay Holekamp is a professor of zoology at Michigan State University.
The research was supported by the Israel Science Foundation (grants 244/19 and 245/19), U.S. Army Research Office (Grant W911NF-17-1-0017), Israel-U.S. Binational Science Foundation (grants 2015088 and 2019156), and National Science Foundation (grants 185
Inherited social networks shape spotted hyena society and survival
In spotted hyena societies, inherited social networks - passed from mothers to offspring - are essential to hyena life and survival, according to a new study. While the structure of animal social networks plays an important role in all social processes as well as health, survival and reproductive success, the general mechanisms that determine social structure in the wild remain unknown. One proposed model, termed social inheritance, suggests that an offspring's social affiliations tend to resemble those of their parents, particularly those of the mother. Previous research has indicated that these inherited social networks may influence social structure across generations in multiple species. Here, Amiyaal Ilany and colleagues evaluate the role of social inheritance in spotted hyena society, which is female-dominated and highly structured. Combining social network analysis and a transgenerational dataset comprised of 73,767 social observations among a population of wild hyenas collected over 27 years, Ilany et al. found that that the social relationships of juvenile hyenas are similar to those of their mothers and that the degree of similarity increases with the mother's social rank. What's more, the results show that the strength of the maternal relationship affects social inheritance and is also positively correlated with the long-term survival for both mother and offspring. According to the authors, the findings suggest that selection for social inheritance might play an essential role in shaping hyena social behavior and the fitness of individual hyenas. "Future work should seek to examine how widely specific social relationships are inherited in a range of population structures and what implications this has for the rate of evolution of the many processes that depend on social network structure," write Josh Firth and Ben Sheldon in a related Perspective.
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CAPTION
A massive study of data collected over 27 years, published today in the journal Science, sheds new light on social networks, rank and survival of spotted hyenas.
Dr. Amiyaal Ilany, a biologist at Bar-Ilan University in Israel, integrates behavioral ecology, network science, and social science, to study broad aspects of social behavior in the wild. As a postdoctoral researcher at the University of Pennsylvania, he developed, together with Dr. Erol Akçay, a theoretical model suggesting that social inheritance - in which offspring inherit their social bonds from their parents, either passively or by copying them - could explain the social networks of multiple species. To test their model Ilany and Akçay forged a partnership with Dr. Kay Holekamp, of Michigan State University. Holekamp had spent the previous 27 years observing wild spotted hyenas in Kenya. Poring over Holekamp's data, which included nearly 74,000 social interactions among the spotted creatures, they were able to show, for the first time on such a large scale, that their model correctly hypothesized that a process of social inheritance determines how offspring relationships are formed and maintained. Their study also elucidates the major role that social rank plays in structuring the spotted hyena clan, and how this affects survival.
CREDIT
Lily Johnson-Ulrich
Among spotted hyenas, social ties are inherited
Massive study of data collected over 27 years sheds light on social networks, rank, and survival of this African species
IMAGE: A MASSIVE STUDY OF DATA COLLECTED OVER 27 YEARS, PUBLISHED TODAY IN THE JOURNAL SCIENCE, SHEDS NEW LIGHT ON SOCIAL NETWORKS, RANK AND SURVIVAL OF SPOTTED HYENAS. DR. AMIYAAL ILANY, A... view more
CREDIT: KATE SHAW YOSHIDA
Social networks among animals are critical to various aspects of their lives, including reproductive success and survival, and could even teach us more about human relationships.
Dr. Amiyaal Ilany, a biologist at the Mina and Everard Goodman Faculty of Life Sciences at Bar-Ilan University in Israel, integrates behavioral ecology, network science, and social science, to study broad aspects of social behavior in the wild. As a postdoctoral researcher at the University of Pennsylvania, he developed, together with Dr. Erol Akçay, a theoretical model suggesting that social inheritance - in which offspring inherit their social bonds from their parents, either passively or by copying them - could explain the social networks of multiple species.
In a study published today in the journal Science, the researchers show, for the first time on such a large scale, that their model correctly hypothesized that a process of social inheritance determines how offspring relationships are formed and maintained. Their study also elucidates the major role that social rank plays in structuring the spotted hyena clan, and how this affects survival.
To test their model Ilany and Akçay forged a partnership with Dr. Kay Holekamp, of Michigan State University. Holekamp had spent the previous 27 years observing wild spotted hyenas in Kenya. The researchers pored over Holekamp's data, which included nearly 74,000 social interactions among the spotted creatures.
"Social affiliations are, indeed, inherited within clusters of hyenas. The plethora of data on spotted hyenas that was collected by Kay Holecamp provided us with a golden opportunity to test the model we developed several years ago," says Dr. Ilany, the lead author of the study. "We found overwhelming evidence that social connections of offspring are similar to those of the mother. A mother who has social affiliations with another hyena can connect her offspring to that hyena and the two, in turn, will form a social bond. Even after the mother-offspring bond itself weakens dramatically, the offspring still remain connected to their mother's friends."
Spotted hyenas live in clans, the size of which depends on the abundance of prey and may vary from only a few individuals to more than a hundred. Life in the clan can be difficult for lower-ranked individuals. They may be excluded and may not get access to food.
"Rank is super important," says Dr. Akçay, who co-authored the study. "Spotted hyena live in a matriarchal society. Those born to a lower-ranked mother are less likely to survive and to reproduce." Descendants of high-class individuals face fewer constraints than descendants of lower-class individuals in choosing their social partners. The researchers found that offspring born to high-ranked mothers copied their mother's bonds more accurately than those born to low-ranked mothers.
Social inheritance plays an important role in survival, and the researchers discovered an association between the two in both mothers and female offspring. There was a positive relationship between offspring survival and social associations that were similar to their mothers, but only in offspring of high-ranked mothers. Mothers of offspring who were more similar to them in social association were more likely to survive to the following year, possibly reflecting a change in maternal relationships as they get older.
The results of this study suggest that social inheritance plays an important role in building the social networks of hyenas and further supports Ilany's and Akçay's hypothesis that in species with stable social groups, the inheritance of social connections from parents is the cornerstone of social structure. In several species successful social integration is associated with higher survival and reproductive success. The results add to this by showing that social inheritance is also associated with both offspring and mother survival.
The researchers note that social network inheritance likely contributes to a group's stability, and also has implications for how behaviors are learned and spread through groups. The study also underscores how factors other than genetics hold sway in key evolutionary outcomes, including reproductive success and overall survival. "A lot of things that are considered by default to be genetically determined may depend on environmental and social processes," concludes Ilany.
CAPTION
A massive study of data collected over 27 years, published today in the journal Science, sheds new light on social networks, rank and survival of spotted hyenas.
Dr. Amiyaal Ilany, a biologist at Bar-Ilan University in Israel, integrates behavioral ecology, network science, and social science, to study broad aspects of social behavior in the wild. As a postdoctoral researcher at the University of Pennsylvania, he developed, together with Dr. Erol Akçay, a theoretical model suggesting that social inheritance - in which offspring inherit their social bonds from their parents, either passively or by copying them - could explain the social networks of multiple species. To test their model Ilany and Akçay forged a partnership with Dr. Kay Holekamp, of Michigan State University. Holekamp had spent the previous 27 years observing wild spotted hyenas in Kenya.
Poring over Holekamp's data, which included nearly 74,000 social interactions among the spotted creatures, they were able to show, for the first time on such a large scale, that their model correctly hypothesized that a process of social inheritance determines how offspring relationships are formed and maintained. Their study also elucidates the major role that social rank plays in structuring the spotted hyena clan, and how this affects survival.
CREDIT
Lily Johnson-Ulrich
