In mammals, males are usually stronger and more competitive than females. Males also show greater inequality in reproductive success – the number of offspring they produce – than females. In spotted hyenas, the opposite is true: reproductive inequality is greater in females than in males. The reason? Female spotted hyenas pass on their social rank and the associated privileges such as priority access to food to their offspring, whereas males do not. These are the findings of a new study on spotted hyenas spanning eight generations across eight clans in the Ngorongoro Crater in Tanzania, carried out by the Ngorongoro Hyena Project of the Leibniz Institute for Zoo and Wildlife Research in Berlin (Leibniz-IZW) and the Institut des Sciences de l'Évolution de Montpellier (ISEM). The study is published in the journal "Science Advances" and may explain why females are the more competitive sex in some species.
In the animal kingdom, not all individuals produce the same number of offspring — and among mammals, this inequality is often greater among males than females. Among sexually reproducing species, males produce numerous, small and motile gametes (sperm), while females produce a small number of large and nutrient-rich gametes (eggs). In mammals, females also bear the physiological cost of pregnancy and lactation. Because females invest far more in each reproductive event than males do, they are more selective about mating. Males benefit more from mating with as many females as possible and therefore compete intensely for access to mates. This leads to conflicts between the sexes and gives rise to sex roles: males want to inseminate as many females as possible and as often as possible, and fight amongst themselves for access to the females, while females are selective and invest heavily in rearing their offspring. These predictions, formalised as the Darwin-Bateman paradigm, have been confirmed across many mammalian species.
The generational effect: Female spotted hyenas show greater inequality in reproductive success than males
Scientists from the Ngorongoro Hyena Project at the Leibniz-IZW and the ISEM analysed the pedigrees of eight spotted hyena clans in the Ngorongoro Crater. This involved over 2,700 individually identified hyenas spanning eight generations and 29 years. The scientists investigated whether the pattern of greater inequality in reproductive success among males could be confirmed. Initially focusing on the annual number of offspring, they calculated inequality in reproductive success separately for males and females. This revealed that, as with most mammals, inequality was greater among males than females. "This initially confirms the Darwin–Bateman paradigm, which predicts and explains greater inequality in reproductive success among males than females", says the study's lead author, Marta Mosna from the Leibniz-IZW.
"Our long-term pedigree enabled us to trace family lineages across generations. It was only when we looked beyond offspring to grand- and great-grandoffspring that the full picture emerged", says Dr Eve Davidian, co-director of the Ngorongoro Hyena Project and a scientist at ISEM. "Reproductive inequality among females increased with every generation we included. Privileged lineages didn't just remain successful — they grew ever larger." High-ranking females produce and successfully rear more offspring than low-ranking females, and the gap widens dramatically when accounting for descendants across generations. In one generation around 10 percent of a clan's offspring are directly descended from alpha females, whereas in the following generation as many as 20 percent are descended from an alpha grandmother. After six generations, virtually all individuals can be traced back to an alpha line, making inequality in long-term reproductive success among females remarkably high.
This pattern is far less pronounced in the paternal line. Consequently, inequality in reproductive success shifts rapidly towards females across generations. Spotted hyenas therefore appear to follow the typical mammalian pattern only when offspring are considered; once grandchildren and great-grandchildren are included, females demonstrate greater inequality than males.
In spotted hyenas, social status influences reproductive success
The scientists of the Ngorongoro Hyena Project attribute this reversal to the social behaviour of spotted hyenas, specifically the social inheritance of privilege along the female line. "In spotted hyenas, clans are organised in a strict dominance hierarchy, with an alpha female at the top. Offspring inherit their social rank from their mother," explains Philemon Naman, field assistant with the Ngorongoro Hyena Project in Tanzania. "A high rank confers advantages on both sexes in the early stages of life, such as priority access to food, faster growth and a higher survival rate." As females usually retain their maternal rank, high-ranking females benefit from these advantages in the long term: they begin reproducing earlier, have shorter intervals between births, and overall have a higher life expectancy than lower-ranking females.
This is where the two sexes diverge. "Males almost always leave to join another clan when they are ready to reproduce, losing their maternal rank in the process", says Dr Oliver Höner, co-director of the Ngorongoro Hyena Project and scientist at the Leibniz-IZW. "As a result, male spotted hyenas, unlike high-ranking females, do not convert a privileged family background into long-lasting reproductive success and lineages that accumulate descendants across generations."
However, this reversal only becomes apparent when an appropriate long-term timescale is used in the data analysis. "If you only measure offspring, you might conclude that there is little inequality among females and therefore weaker competition among them, and that males are the more competitive sex", explains Mosna. "However, if you measure across generations, you see the opposite – finally explaining why females are the more competitive sex among hyenas!"
Female-biased competition and reproductive inequality have also been observed in other species – for instance, in seahorses, where males provide parental care, or in meerkats, where reproduction is monopolised by one dominant female. "This study identifies a third route to the same outcome: the inheritance of social privileges along the female line", concludes co-author Dr Alexandre Courtiol from the Leibniz-IZW. This form of maternal inheritance also exists in other species. Whether it leads to similar reversals in reproductive inequality is a question for future research.
