Nature, Nurture, and the Spotted Hyena

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Nature, Nurture, and the Spotted Hyena

SciMed - Biology

TS-Si News Service

Tuesday, 21 April 2009 21:00

Fairfax, VA, USA. Discussions of gender are often uninformed by findings from the physical sciences, but the situation has begun to change.

Hard research into the interrelationship of nature and nurture now offers testable hypotheses that distinguish between sex and gender, pointing toward more comprehensive theorizing that is unaffected by value judgements.

Such investigations include systematic study of developmental proceses and isolation of critical variables to measure and assess their interplay in an evolutionary context.

The spotted hyena (Crocuta crocuta, or "laughing" hyena) is a rigorously-studied animal; the research findings, particulary those involving female dominance, have clarified issues while raising new and interesting opportunities for further research.

From an evolutionary perspective, the term dominance can refer to the genetic preeeminance of one or more traits over others. From a behavioral perspective, it can refer to the state that exists when one person or group has power over another, with the implied authority to issue orders and/or make decisions. Generally, researchers in

molecular biology and biochemistry view physiological factors as the primary cause of dominant characteristics (while allowing an important role for the

evolution of genetic dominance). [Cf. Note]

A procession of research studies have resulted in an improved understanding of female dominance in hyenas, shedding light on developmental and behavioral issues with potentially wide application to the study of other mammals.

Biology and Gender Roles

The social sciences and humanities generally view an individual's gender role as the set of perceived behavioral norms that are associated with females or males. The specific role descriptions tend toward stereotypical attitudes and behaviors (e.g. women cook, clean, and avoid sports; men fix cars and play sports). Note that, for most social groups or systems, the terms sex and gender are often used interchangeably.

This usage tends to isolate sex and gender from biological imperatives, even when the analysts involved initially concede that an individual's gender role involves the transformation of biological sexuality into social practices. Further analysis drifts toward an exclusive focus on societal influences, crediting femininity or masculinity to gender as a personal choice or socially imposed restriction.

Patterns in Nature

Overall, hyenas are most closely related to the family that includes mongooses and are more closely related to cats than dogs. C. crocuta is the largest hyena species of all, standing up to 3 feet tall and weighing up to 185 pounds. Primarily native to sub-Saharan Africa and the Congo basin, it thrives in a variety of habitats that range from hot and arid lowland areas (northern and southern ranges) to mountainous terrains in East Africa and Ethiopia that are quite cold.

Protecting Hyena Cubs

Hyena cubs are at risk after weaning because their massive skulls and jaws don't fully develop until sexual maturity. Kay Holekamp and associates theorize that lengthy development and intense feeding competition prompts development of dominant female behaviors.

Photo courtesy of Kay Holekamp (Univeristy of Michigan).

Kay Holekamp is widely considered one of the top authorities on the Spotted Hyena. A zoologist, she teaches at Michigan State University, with frequent trips to Masai Mara in Kenya for field work. Her partner, the neurobiologist Laura Smale (also a professor at MSU), is an occasional collaborator. She is known by many in Masai Mara as "Mama Fisi"(fisi is Swahili for hyena).

Photo courtesy of the University of Michigan.

The spotted hyena is a skilled hunter that derives the majority of its nourishment from live prey, despite their popular misperception as a scavenger (hyenas can eat things that would sicken or kill many other species). They can bring down prey several times their own size, with powerful jaws that crack open giraffe leg bones up to 3 inches in diameter.

The hyenas live in a complex social system, with clans that number up to 90 members. The females rule, making them rare among mammals and unique among carnivores. In human society and many animal societies, social status is crucial — it determines access to resources, survival and reproductive success. “In highly developed mammalian societies such as spotted hyenas, social status is even more important to survival and reproductive success than environmental factors, predators or pathogens” says Prof Heribert Hofer from the Leibniz Institut für Zoo und Wildtierforschung (IZW) in Berlin, Germany.

As a result, parents may attempt to pass on their status to their offspring. Such ‘rank

inheritance’ has been observed in a number of mammalian species, including many primates and the spotted hyena (Crocuta crocuta, or "laughing" hyena).

However, that is not the end of the story. Hyena cubs take a long time to develop the skulls that house their jaws, with full development deferred until after sexual maturity.

This raises questions about how spotted hyenas, especially females, protect their young while maintaining strong clan relationships and social cohesion.

Androgens Matter: The Effects of Hormones on Hyena Development

Among spotted hyenas, hormones give cubs a powerful head start. A report in Nature [C1] established that high-ranking, dominant spotted hyena mothers pass on high levels of androgens to their offspring that make cubs more aggressive and sexually vigorous.

Kay Holekamp is a zoology professor at Michigan State University (MSU). She conducted the research with her former graduate student Stephanie Dloniak and Jeffrey French from the University of Nebraska. The high

hormone levels “.. are gifts a mom can give to her baby,” said Holekamp. “She can manipulate her offspring’s behavior and help her kids to survive and reproduce successfully by transferring status-related traits via prenatal hormone exposure.”

This study demonstrates that alpha females have higher levels of androgen during the final stages of pregnancy than lower-ranking group members. With this benefit, the cubs are more likely to survive, thrive and reproduce.

The research resulted from nearly two decades studing wild spotted hyena populations in Kenya. The paper outlines the first instance where researchers have shown that a female mammal’s hormones can influence her offspring’s behavior and appearance.

Androgen is just one of the many hormones traveling across the placenta to the developing fetus. This hormone mediates masculine characteristics like aggression, muscle development and male-typical sexual behavior.

But it’s not just the male cubs that stand to benefit from the maculinizing effects of androgens. Females gain just as much. Normally, when it comes to muscle mass, aggressive behavior and dominance, males have the benefit, but female hyenas benefit from a striking reversal.

The sex roles in spotted hyenas are completely reversed from those in most mammals: females are larger and more aggressive than males when competing for limited resources and dominate the members of their social group. “You don’t find many mammals where the female is the boss,” Holekamp said.

Females look so much like males that an observer may have difficulty differentiating the sexes. A female hyena’s genitals have evolved into something that looks more like a penis than a vagina. A spotted hyena’s vaginal canal makes a hairpin turn and exits the body like a penis. The opening of the vaginal canal is at the end of an elongated clitoris, nearly six to seven inches in an adult, that looks remarkably like a penis, Holekamp said. Not surprisingly, ancient people, like the Greek philosopher Aristotle, thought hyenas were hermaphrodites.

Holekamp and her colleagues speculate that the behaviors attributed to high levels of prenatal androgens may be evolution’s way of offsetting the negative consequences associated with mating and giving birth through a penis-like structure.

The characteristics of the genitalia are responsible for some obvious anatomical challenges that arise when it’s time for a hyena to mate and give birth. Mating is a tricky manuever: a male must position himself at just the right angle to enter the female’s clitoris. If the match is successful, a mother hyena will give birth to each of her 2-pound cubs through the elongated clitoris, which doubles its diameter from one to two inches for the occasion.

The physical characteristics and behaviors handed down from alpha moms to their babies may be helpful in understanding how this unique genitalia evolved and why it works.

Mating that culminates in pregnancy and successful rearing of young is contingent on a female’s ability to secure food resources. More aggressive females are better able to compete for food when hyenas squabble over carcasses of gazelles, wildebeest and zebras, which are their main prey.
Young males exposed to higher levels of prenatal androgen exhibit mounting behaviors more often than the males born to lower-ranking females. In other words, they get more practice at the difficult art of hyena mating.

“It’s really weird genitalia, but it seems to work. Although giving birth through a ‘penis’ isn’t a trivial problem.” Holekamp said. “All her female-typical behaviors are there — she’s been masculinized without being defeminized.”

Sex Role Reversal in Spotted Hyenas: Female Dominance Theory

Male hyenas have found that getting between a female hyena and her cubs at dinner time can be hazardous to the males' health. Females rule among spotted hyenas, making them rare among mammals and unique among carnivores. After more than 20 years of closely studying generations of the ferocious, yet social creatures, Kay Holekamp and her colleagues now believe they know why.

The researchers published their findings in a paper that appears in the Proceedings of the Royal Society B. [C2] They theorize that the length of time it takes for the massive skulls and jaws of hyenas to mature in youngsters — combined with the intense feeding competition typical of hyena clans — prompt female family members to develop dominant behaviors.

Holekamp was joined in her research by Heather Watts, the report's lead author, and Jaime Tanner, both former Holekamp laboratory graduate students. Associate zoology professor Barbara Lundrigan, curator of mammalology and ornithology at the MSU Museum, lent her expertise on skull development and helped develop and test the group’s new

hypothesis using many of the museum's 70-plus known-age hyena skulls.

Bottom line? "Mothers have to compensate with aggression for the handicaps their kids are experiencing during feeding," she said. Hyena cubs are at particular risk after they are weaned, she said, because their skulls don't fully develop until after sexual maturity.

Conflict Over How Spotted Hyenas 'Inherit' Social Status

An international team of scientists from IZW and the University of Sheffield, UK, have taken a more orthodox approach when addressing the question of how social status is inherited in the spotted hyena, one of the most social of all mammals.

In a study published recently in Behavioral Ecology, [C3] the scientists used observations during the last 20 years of rare cases of adoption among hyenas in the Serengeti and at Ngorongoro Crater in Tanzania. They combined these observations with molecular techniques to identify genetic mothers and evaluate hyena mothers to see if they pass on their social status by supporting their young during social interactions with other group members.

“In spotted hyenas, surrogate mothers adopt young cubs soon after their birth. The adopted cubs obtained a rank at adulthood that was similar to and just below the rank of their surrogate mother. In contrast, the rank of adopted offspring was unrelated to the rank of their genetic mother” says Dr. Marion East from the IZW.

East says “This is consistent with the idea that maternal behavioural support determines rank inheritance.” At a glance, the study results appear to be inconsistent with two of the alternative hypotheses to explain rank inheritance in social mammals:

mothers might transfer genes that cause their offspring to be as competitive as themselves; or
maternal status might determine the concentration of maternal androgens (testosterone) that a fetus is exposed to, and this exposure in turn might make offspring become as competitive as their mother.

Oliver Höner from the IZW has stated that “These hypotheses would predict a relationship between the rank of adopted offspring and that of their genetic mother, but we found no evidence of such a relationship.” These assessments are based on the idea that both hypotheses project a determined outcome with no room for socialization. That is, there should be a one-to-one correspondence between the exact social rank of the mother and the offspring, whether adopted or not.

This assessment is open to dispute. If it were true, <em>all</em> offspring would be dominant and have same social status, ignoring the fact that dominant females (dominant over males) are themselves subject to clan hierarchy. Moreover, genetic and hormonal endowments provide the physical basis for survival and the acquisition of knowledge. [Cf. Note]

Socialization, within physical constraints, affects all female spotted hyenas. In fact, the IZW study did demonstrate that young heyenas "learn" during adolescence. They find out which group members they can dominate when their adoptive mother helps them win contests against group members that are subordinate to the mother. When they reach adulthood, they defend this position and benefit from the "silver-spoon effect".

Because social dominance provides fitness benefits in spotted hyenas, they obtain the benefits associated with this position. However, they wouldn't be in a position to exploit their social conditioning without first benefiting from their physical endowment as cubs.

Implications

Increasingly, the findings of biological science have changed the baseline understanding of behavior, leading to a more fact-based appreciation of gender role development. Scientists recognize that socially enforced rules and values are overlaid on innate mammalian capabilities, leading in turn to a better understanding of how (and how much) gender depends on biological sex.

The ability to develop robust theories that generate testable hypotheses offers a substantial change in gender studies.

NoteDebates over dominance have a long history. Ronald Fisher made the central argument for genetic dominance in his papers and eventual book, The Genetical Theory of Natural Selection (1928). Fisher's central argument was that modifier genes act upon other genes to make them dominant or recessive; these genes are then subject to natural selection. Sewall Wright and J.B.S. Haldane argued that dominance is based on physiological factors. Subsequent research - and clarification of the underlying mechanisms - has resulted in a synthesis that favors

physiology, but allows for genetic explanatyions in some circumstances.

Citations[C1] Rank-related maternal effects of androgens on behaviour in wild spotted hyaenas. J. A. French, K. E. Holekamp, S. M. Dloniak. Nature 440: 1190-1193 (27 April 2006). doi: 10.1038/nature04540 Letter.

Abstract

Within any hierarchical society, an individual's social rank can have profound effects on its health and reproductive success1, 2, and rank-related variation in these traits is often mediated by variation in endocrine function2. Maternal effects mediated by prenatal hormone exposure are potentially important for non-genetic inheritance of phenotypic traits related to social rank3, and thus for shaping individual variation in behaviour and social structure. Here we show that androgen concentrations in wild female spotted hyaenas (Crocuta crocuta) are higher during late gestation in dominant females than in subordinate females. Furthermore, both male and female cubs born to mothers with high concentrations of androgens in late pregnancy exhibit higher rates of aggression and mounting behaviour than cubs born to mothers with lower androgen concentrations. Both behaviours are strongly affected in other mammals by organizational effects of androgens4, and both have important effects on fitness in hyaenas. Therefore, our results suggest that rank-related maternal effects of prenatal androgen exposure can adaptively influence offspring

phenotype in mammals, as has previously been shown to occur in birds. They also suggest an organizational mechanism for the development of female dominance and aggressiveness in spotted hyaenas, traits that may offset the costs of extreme virilization.

[C2] Post-weaning maternal effects and the evolution of female dominance in the spotted hyena. Heather E Watts, Jaime B Tanner, Barbara L Lundrigan, and Kay E Holekamp. Proceedings of The Royal Society B Biological Sciences Epub ahead of print: 2009. doi: 10.1098/rspb.2009.0268.

Abstract

Mammalian societies in which females dominate males are rare, and the factors favouring the evolution of female dominance have yet to be clearly identified. We propose a new hypothesis for the evolution of female dominance and test its predictions with empirical data from the spotted hyena (Crocuta crocuta), a well-studied species characterized by female dominance. We suggest that constraints imposed by the development of a feeding apparatus specialized for bone cracking, in combination with the intensive feeding competition characteristic of spotted hyenas, led to the evolution of female dominance. Specifically, we propose that protracted development of the feeding apparatus in young hyenas led to selection for increased aggressiveness in females as a compensatory mechanism for mothers to secure food access for their young after weaning. Our analyses yielded results consistent with this hypothesis. Morphological and behavioural measurements indicate that skull development is indeed protracted in this species; spotted hyenas do not achieve adult skull size or feeding performance capabilities until after sexual maturity. The period between weaning and completed skull development is particularly challenging, as indicated by high mortality. Finally, maternal presence between weaning and full skull maturity, as well as the relative ability of females to aggressively displace conspecifics from food, are important determinants of offspring survival.

Keywords:development, female dominance, life history, mammals, skull, spotted hyena.

[C3] Maternal effects on offspring social status in spotted hyenas. Marion L. Easta, Oliver P. Hönera, Bettina Wachtera, Kerstin Wilhelma, Terry Burkeb and Heribert Hofera. Behavioral Ecology Epub ahead of print: February 27, 2009, doi: 10.1093/beheco/arp020.

Abstract

Social status is an important phenotypic trait that determines fitness-relevant parameters. In many mammalian societies, offspring acquire a social position at adulthood similar to that held by their mother ("rank inheritance") and thus obtain fitness benefits associated with this status. Mothers may influence the rank of their offspring at adulthood in at least three distinct ways. Firstly, the direct genetic inheritance of maternal traits that influence resource holding potential might predispose offspring to obtain a rank similar to that held by their mother. Secondly, the prenatal maternal environment might influence offspring rank if fetal exposure to maternal androgens is related to maternal status and affects offspring competitiveness. Thirdly, maternal behavioral support, a component of the postnatal maternal environment, may help offspring dominate individuals subordinate to their mother, thereby assisting offspring to acquire a rank similar to that of their mother. Here, we simultaneously test predictions derived from these three potential maternal effects on offspring rank acquisition at adulthood, using cases of offspring adoption in the spotted hyena Crocuta crocuta. We demonstrate that the rank of adopted offspring at adulthood was similar to that of their surrogate mother and that the competitive ability of offspring at adulthood was best explained by postnatal maternal behavioral support.

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Last Updated on Tuesday, 21 April 2009 21:06

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