Strong immunity=low fertility

A study in wild sheep may help explain why natural selection has not eradicated weak or self-destructive immune systems

By | October 28, 2010

A fluctuating trade-off between reproduction and survival in a feral population of Soay sheep may resolve the age-old question of why natural selection has failed to eradicate genes for both infection-prone and self-assailing immune systems.
linkurl:Soay sheep (Ovis aries);http://www.flickr.com/photos/hippie/2633863104/
Photo courtesy of Philippa Willitts
The potential answer, published in Science this week (29th October), comes from the nascent field of ecoimmunology, which examines how different levels of antibodies in the blood of wild animals can influence their ability to survive and produce young. Specifically, the authors found that, among a population of isolated, wild sheep, individuals with higher levels of antibodies associated with autoimmunity in other species were more likely to survive harsh weather conditions, but also reproduced less. Consequently, the benefits of high immunity, such as quick and efficient riddance of infection, may come with a cost -- less energy for reproduction. "This paper reveals that more [antibodies] might not always be better, and that to understand the evolution of immune systems, it will be critical to study them in free-living, outbred organisms," linkurl:Lynn Martin,;http://lbmartin.myweb.usf.edu/Martin_lab_at_USF/People.html an ecoimmunologist at the University of South Florida, who was not affiliated with the study, said in an email to The Scientist. Researchers have found that feral rodents can hold comparatively high concentrations of antibodies in their blood, but, mysteriously, autoimmunity diseases such as type 1 diabetes and lupus are only seen in humans and lab, domestic, and captive mammals, said linkurl:Andrea Graham,;http://www.princeton.edu/eeb/people/display_person.xml?netid=algraham&display=All an evolutionary biologist at Princeton University and first author on the study. There was "this nagging question of whether autoimmunity was some weird freak of captivity," added linkurl:Andrew Read,;http://www.cidd.psu.edu/people/afr3 evolutionary biologist at Pennsylvania State University, who did not contribute to the study. Using blood samples collected every August for 11 years from the Soay sheep population on Hirta, an island in the St. Kilda archipelago of Scotland, Graham and colleagues from the University of Edinburgh in Scotland measured the concentration of antinuclear antibodies (ANAs), or autoimmune antibodies that attack the contents of the cell's nucleus as if it were foreign material. They then compared these levels to other variables of fitness such as survival and reproduction. Researchers found that adult females with higher levels of ANAs lived longer by surviving more bitterly cold, parasite-infested winters. However, these same females were less likely to have babies the following spring. The correlation was only present during particularly harsh winters, however, when sometimes nearly 50 percent of the population died, suggesting heterogeneity in immune response is produced by natural selection acting on an ever-changing environment.
A female Soay sheep in snow on the Scottish island of Hirta, St. Kilda
Image courtesy of Gina Prior
Ewes with high levels of ANAs also produced young with higher chances of survival through the next winter than young born to mothers with weak immune systems, suggesting a genetic basis for the varied immune responses in the sheep population. "Immune response is only one part of the fitness component," said linkurl:Peter Hudson,;http://www.personal.psu.edu/pjh18/ a disease ecologist at Pennsylvania State University, who was not affiliated with the study. "When [an individual] is not being exposed to pathogens, then high immune response could be too costly." According to the results, when parasite prevalence is low and food is abundant, individuals with low immune responses will have the highest fitness because they will have the energy to produce the most young in the shortest period of time. But when the threat of infection is high and the winters are brutally frigid, individuals with high immune responses will survive and live on to have more children, while others die off. Thus, these trade-offs exhibited by the Soay sheep can account for their heterogeneity in immune response. Read and Martin agreed that the next step is to experimentally manipulate antibody response in large populations to discover whether a causal, rather than correlational, relationship is present in this survival-reproduction trade-off. The field of ecoimmunology "has been a controversial field because it's really hard to decide what to measure without a history [of the population]," noted Read. This study demonstrates its potential benefits, however, Graham argued. "I firmly believe that we wouldn't have been able to find out such cool things about the immune system without this long study on the Soay sheep," she said. "Now that we understand all the nuts and bolts of the immune system [from traditional immunology], we can go on to try to understand it in the real world, because that's what really matters." A. Graham et al., "Fitness Correlates of Heritable Variation in Antibody Responsiveness in a Wild Mammal," Science, 330:662-65, 2010.
**__Related stories:__***linkurl:Following the flock;http://www.the-scientist.com/blog/display/55656/
[23rd April 2009] *linkurl:Embryonic origins of autoimmunity;http://www.the-scientist.com/blog/display/54377/
[26th February 2008] *linkurl:Is autoimmunity like cancer?;http://www.the-scientist.com/blog/display/54273/
[2nd February 2008]

Comments

Avatar of: Leena Liljedahl

Leena Liljedahl

Posts: 1

October 28, 2010

Maybe there is a very easy answer to the question on why we never see autoimmune diseases like Type 1 diabetes in wild animals, but only in human and animals under human care - they die, and therefore are never seen to breed.\nI guess another reason for high immunity - low fertility could be that the first cell canĀ“t be fertilized, it sees everything as an intrudor, which it kills.
Avatar of: Gil Lawton

Gil Lawton

Posts: 42

October 28, 2010

It does not seem to me that all kinds of immunity share the same characteristics or repercussions. The argument that energy is more limited for some species than others might be valid in any event. But to lump, say, immunity to cold with immunity to a given bacterium or virus is an immensely wide brush to paint with, don't you think?\n\nIndeed, the amount of energy required to produce antibodies is not always great. But I would hesitate to think of immunity as being a single challenge to reproduction, whether it be immunity from predation, immunity from infection, immunity from man-made toxins, immunity from climate extremes, immunity from starvation... that's a lot of stuff to cram into a single bag. Isn't it?
Avatar of: Mike Waldrep

Mike Waldrep

Posts: 155

October 28, 2010

Interesting!
Avatar of: michele marcus

michele marcus

Posts: 1

October 28, 2010

These observations are very interesting but I'm puzzled by the authors' speculation that sheep with high immunity don't have enough "energy" left to reproduce. A simpler and more biologically plausible explanation is that females with a strong immune system reject the developing fetus. Women with ANA have a high rate of spontaneous abortion. Pregnancy requires a temporary tamping down of the immune system.
Avatar of: Alexandru Cosciug

Alexandru Cosciug

Posts: 16

October 28, 2010

I know that the mitochondria give the sperm motility.\nQuestion: does the immunity increasing reduce the natural activity of mitochondria?\n
Avatar of: Hilary Butler

Hilary Butler

Posts: 15

October 28, 2010

This comment here is highly suspect:\n\n***\n"Now that we understand ALL THE NUTS AND BOLTS of the immune system [from traditional immunology], we can go on to try to understand it in the real world, because that's what really matters." ***\n\nThe real world is what really matters, but traditional immunology knows just about nothing about the intricacies of the inate immune system; OR how it meshes with the rest of the immune system.\n\nImmunology as a "speciality" is actually a colander with large black holes, and is defined more by what it doesn't know than what it does... so to say such a thing is quite extraordinary.\n\nRe the comment about type 1 diabetes. Indigenous tribes with no access to sugar or refined carbohydrates, who eat a wide variety of native fruits and vegetables about which we know little, and a huge variety of various local protein sources, also have no indigenous "knowledge" about type 1 diabetes either. Does that mean that children or people die off young, or does that mean that the highly "abnormal" eating patterns of today, are part of the problem?\n\nIn cultures long gone but who had a long history of written records, what is said about deaths which would now be compatible is untreated type 1 diabetes? \n\nThere is malnutrion and bad nutrition, and both can have different, and dire consequences.\n\n
Avatar of: anonymous poster

anonymous poster

Posts: 1

October 29, 2010

Interesting article. However, it is not that surprising. The idea of a trade-off between the cost of mounting a strong immune response and components of individual fitness has been around for some time. I vaguely recall a study about mites and lizards illustrating this point.
Avatar of: Giuseppe Damiani

Giuseppe Damiani

Posts: 3

November 4, 2010

In complex animals, the acquired immunity regulates the selective proliferation of the cells with adaptive mutations during the physiological responses to stresses. The same immunotrophic process allows the maternal selection of embryos with adaptive mutations. The fetal-maternal incompatibility counteracts the negative aspects of Darwinian natural selection and maintains the metabolic biodiversity of animal populations. The increased knowledge of relationships among metabolism, epigenetic systems, genome plasticity, and acquired immunity, supports the idea that these processes could provide a form of Lamarckian adaptive evolution in response to environmental stresses.\n\nDamiani G. - The Yin and Yang of anti-Darwinian epigenetics and Darwinian genetics. Riv Biol. 2007 Sep-Dec;100(3):361-402.\n\nhttps://sites.google.com/site/binarytheoryofeverything/relevant-papers

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