Silver Spoon Hyenas: Maternal Social Status Affects Male Reproductive Success

Early developmental experiences can have significant implications for the growth, behavior, survival, and reproductive success of an individual. In many species, one of the most important factors that affects an individual's early development is the maternal environment. However, mothers not only provide an environment for their offspring, but also half of their genes, making it difficult to separate the effects of nature and nurture when investigating developmental outcomes in the offspring. Moreover, because male mammals usually disperse from the social groups into which they were born, it is difficult to determine how the maternal environment might influence the reproductive success of sons.

In species with marked sexual dimorphism, such as the red deer (Cervus elaphus), male fitness is related to overall body size and fighting ability. In this case, it is somewhat obvious that a mother of high social status who is able to provide her sons with more resources will result in larger, stronger males. However, in species with less sexual dimorphism, in which male reproductive success is not determined on the basis of body size or fighting ability, it is not clear whether the social status of the mother provides any real benefit to the son, in terms of his future reproductive success. The spotted hyena (Crocuta crocuta) is one such species.

The spotted hyena is a large carnivorous species that lives in "highly structured, female-dominated social groups called clans," in which access to resources is determined on the basis of social status. For that reason, females of high status have higher reproductive value and success than low-status females. In these clans, females generally spend their lives in the group into which they were born, which daughters acquiring a position in the dominance hierarchy close to and below that of their mother. They retain their social status into adulthood, as long as they retain the support of a close female relative. By contrast, male offspring typically leave the clan into which they were born after some time, and immigrate into another clan. However, they do not bring their social status with them. Instead, they must start at the bottom of the social ladder, and as higher-ranking males emigrate to other clans, or die, their social status can increase.

While female reproductive success is ultimately based on the social status of the mother, male reproductive success is dependent on how well the males conform to the preferences of the females. Indeed, females have complete control over who gets to mate with them.

Given the particular features of the social structure of these hyenas, the mechanism by which maternal social status affects the reproductive status of the daughters is quite clear. However, what is less clear is whether the social status of the mother can affect the reproductive status of her sons, especially since his privileged status does not transfer with him to his new clan upon emigration. Previous research of juvenile hyenas raised by adoptive mothers found no evidence of direct maternal genetic effects on the social rank of adopted offspring at adulthood. If a hyena was adopted by a high-ranking mother, he or she retained the high status of the mother irrespective of genetics. Thus, direct genetic effects were ruled out, and the researchers turned to environmental mechanisms.

Using data from a fourteen year study of all members of eight hyena clans resident in the Ngorongoro Crater in Tanzania, a group of researchers from Germany and the UK tested whether maternal social status influenced a number of factors: (1) the growth rate of the suns during infancy and early childhood, (2) their likelihood of immigration into the optimal clan in terms of potential reproductive success, (3) their age at first reproduction, and (4) the duration of residency in the new clan after immigration. They also investigated whether females preferred to mate with sons of high-ranking mothers. Their overall finding was that maternal social status did significantly contribute to the reproductive success of sons. But how?

They found that maternal social status strongly influenced the physical growth of their sons during the first six months of life. This makes good sense, as the hyena cubs are entirely dependent on milk supplied by their mothers. High-ranking sons grew on average of 85.2 grams per day, which was significantly faster than mid-ranking sons (71.4 grams per day), and low-ranking sons (66.7 grams per day).

Prior research had shown that males who immigrated into clans with the highest number of young females (between 1 and 5 years of age) have higher long-term reproductive success than other males, because young females prefer mating with new immigrants. Is it possible that maternal social status influenced the likelihood of sons to join the optimal clan, with the highest number of young females? The researchers ranked the eight clans based on the number of young females, and counted the number of immigrations into each clan, and compared it with the expected number of immigrations if immigration occurred randomly. Sons of high-ranking mothers routinely chose the clans offering the highest long-term reproductive benefit, and this was statistically different from what would be expected by chance. The immigration patterns of sons of low-ranking mothers was not different from what would be expected by chance; some of the males wound up in optimal clans, but just as many other males wound up in sub-optimal clans. Furthermore, even after immigrating, sons could return to their childhood clan, and upon returning would be treated according to the social status of their mothers. Even after leaving home, the sons of high-ranking mothers could return and again enjoy preferential access to resources.

Maternal social status also influenced the age at first reproduction for the 48 sons that had at least one offspring during the study. After controlling for several other variables in a mathematical model, sons of high-ranking mothers fathered their first offspring at an average age of 4.85 years, which was significantly younger than sons of mid- or low-ranking females.

The evidence demonstrates that maternal social status influenced two important variables: the sons' immigration into a high-quality clan, and the age at which their sons started to have cubs of their own. The earlier age at which sons of high-ranking mothers begin to reproduce increases the overall likelihood of a male to reproduce before dying. More importantly, however, it increases the male's contribution to the overall growth of the population, because offspring from earlier reproduction can contribute to population growth earlier as well.

What does this mean exactly? During the fourteen years of this study, the hyena population increased at an average annual rate of 8.5%, which meant that the annual contribution of any given individual male to that population growth decreased over time; the percentage of the population carrying an individual male's genes would be smaller and smaller each year as the total number of individuals increased. Since sons of high-ranking mothers began reproducing earlier than sons of mid- of low-ranking mothers they were at a distinct reproductive advantage. In a system in which an individual's contribution to population growth decreases each year, it is advantageous to begin reproducing earlier.

In spotted hyenas, females of high status have increased access to resources, and as a result, their sons grow faster and likewise have increased access to resources until they immigrate, as well as for a considerable amount of time after they've left their childhood clan. The researchers concluded that this "may permit sons of high-ranking females to invest more time and energy than sons of low-ranking females in building friendly relationships with females of the new clan, a tactic that increases a male's chance of siring offspring with these females." Since the sons of high-ranking females can return home to eat, they are able to spend most of their time courting females, while sons of lower-ranking females must spend that time foraging instead. Ultimately, the combined opportunities to mate earlier and with more females allows sons of high-ranking mothers to contribute substantially more to the growth of the hyena population than can sons of lower-ranking mothers.

The moral of the story, of course, is that to increase your reproductive fitness, you should leave home early but return often to raid the fridge. Which is exactly what I already do.

Höner, O., Wachter, B., Hofer, H., Wilhelm, K., Thierer, D., Trillmich, F., Burke, T., & East, M. (2010). The fitness of dispersing spotted hyaena sons is influenced by maternal social status Nature Communications, 1 (5), 1-7 DOI: 10.1038/ncomms1059