BEACON Researchers at Work: Does sociality influence disease resistance?

This week’s BEACON Researchers at Work blog post is by MSU graduate student Katy Califf.

Katy Califf and hyenaI’m generally interested in how genetic diversity and behavior influence each other in wild populations of mammals, particularly in the realm of disease ecology. More simply, how do genetics influence behavioral decisions such as where to live, with whom to cooperate, and with whom to mate? Then, over time, as these decisions are made, what does the genetic population structure look like? When you think about it, a lot of these decisions come down to questions about pathogen resistance. If I live here, will I be safe? If I eat this, will I get sick? If I have kids with this individual, will they be healthy? 

Obviously, most of these decisions are not conscious ones for many animals. So the next question is: how are these decisions made? Even if you’re not a scientist, you probably know that in the wild, we usually see related individuals living together, and unrelated individuals mating. This is because of genetic diversity. Related individuals are genetically similar and will often cooperate, as they gain what we call “inclusive fitness” by increasing the survival of individuals who share some of the same genes.  Similarly, it is more beneficial to mate with unrelated individuals than to mate with closely related individuals, because this increases the genetic diversity of the offspring. There are many reasons why this is beneficial, but the one I am most interested in is the possibility that genetic diversity is an important determinant of disease resistance. In fact, many biologists believe that sex evolved as a mechanism to increase genetic diversity, largely in response to constantly evolving pathogens.

This leads us to another question: how do animals know to which animals they are related? Sometimes, they simply know through experience. But in the wild, animals often encounter related individuals that they’ve never met before. Evolution has favored mechanisms for recognizing these individuals, often through the sense of smell. Many wild animals demonstrate these unconscious preferences. 

The well-known “t-shirt study” demonstrates how preferences based on genetic information might operate.  In the 90’s, Wedekind & Furi asked female students to sniff sweaty t-shirts that males had worn for several days, and tell the researchers which odors they preferred. Interestingly, the females preferred shirts that had been worn by men who were genetically dissimilar from them at a group of genes known as the major histocompatibility complex, or MHC. When these females were taking an oral contraceptive, this preference was reversed. These same patterns have been seen in other species as well. The researchers concluded that this preference arises because, when the females are able to become pregnant, they prefer the odor of males that will make better mates, genetically speaking. And when they are unable to become pregnant, they prefer the odor of males that are more likely to be kin, and thus more likely to be reproductive helpers. 

MHC genes are critical to disease resistance in vertebrates. The molecules encoded in these genes recognize foreign pathogens in the body and present them to immune system cells, thereby initiating immune response. Diversity in MHC genes has been linked in many species to increased reproductive success, decreased parasite loads, and enhanced disease resistance. However, it’s not yet completely clear how the MHC genes influence odor.

Photo by Andy Flies

As a graduate student in Dr. Kay Holekamp’s lab, I am currently addressing questions related to MHC diversity in a highly social carnivore, the spotted hyena (Crocuta crocuta). The Mara Hyena Project, run by Dr. Holekamp, has been studying spotted hyenas in the Masai Mara National Reserve in Kenya since 1988. Spotted hyenas are unique among carnivores in that females are socially dominant to all breeding males. Females have complete control over mating, due to their highly masculinized genitalia. Since female choice is essentially absolute in this species, it’s a great system in which to ask questions about the underlying mechanisms of mate choice.  In addition, research has shown that hyenas have a particularly robust immune system. They regularly test positive for many diseases that have caused massive mortality in sympatric carnivores, yet hyenas rarely get sick, and their disease related mortality is much lower than that of other carnivores. While hyenas are exceptionally adept hunters, they also regularly feed on carrion, and they have specific adaptations to break open large bones. These feeding habits might expose them to certain types of parasites or pathogens to which other carnivores are not exposed. 

First, I wanted to know just how diverse the MHC genes are among spotted hyenas. I have sequenced 3 genes in hyenas that have been linked to various fitness measures in other species, and have found that spotted hyenas do indeed exhibit evidence of strong positive selection and high diversity at their MHC loci. I am now analyzing several years of pedigree data to determine whether females tend to mate with males that differ from them at these loci more than would be expected by chance. If immune system diversity is important to hyenas, I would expect them to be mating with individuals that differ from them at MHC. However, it is also possible that all spotted hyenas are already so diverse that something other than mate choice is driving this diversity. 

I have also looked at MHC diversity in a closely related hyena species, the striped hyena (Hyaena hyaena). The striped hyena is a more “typical” mammal than the spotted.  There are no sex role reversals in this species, and they tend to be solitary or live in small family groups. However, I find levels of MHC diversity in this species that are just the same as those in spotted hyenas. This leads me to believe that there is some evolutionary force in hyenas that is more important in maintaining MHC diversity than sexual selection. Unique traits shared by both of these hyena species are the ability to crack bone and feed on carrion. Perhaps the pathogens encountered via this feeding ecology are more important in hyenas than other carnivores, and this may be what is driving variation. 

I am currently sequencing MHC genes in the remaining 2 extant species in the Hyaenidae family to test this hypothesis. The brown hyena (Parahyaenea brunnea) also cracks bone and feeds on carrion. However, the aardwolf (Proteles cristata) is a diminutive hyena that feeds only on termites. If the above hypothesis is correct, in the brown hyena I would expect to see levels of MHC diversity similar to the spotted and striped hyenas, whereas I would expect to see lower levels of diversity in the aardwolf. Either way, these data will further clarify the picture of evolution at MHC genes in hyenas. Stay tuned!

For more about Katy’s work, you can contact her at califfka at msu dot edu.

About Danielle Whittaker

Danielle J. Whittaker, Ph.D. Managing Director of BEACON
This entry was posted in BEACON Researchers at Work and tagged , , , , , . Bookmark the permalink.

Comments are closed.