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Evolutionary Arms Race:
Competing Interests in Male and Female Genomes

Siblicide and deadly sperm — both of these are just two examples of wide-ranging and downright creepy consequences of competing interests of males and females. "Battle of the sexes" is a cliché; however, it is fascinating to see this battle play out on the level of genes. Dawkins wrote about 'selfish genes' in 1976 — and since then, many examples of genes that behave to the detriment of the organisms that carry them had been discovered. This is especially true of the situations where male and female genomes are at odds.

There is strong evidence that the competing interests lead to a much quicker evolution of reproductive proteins, compared with pretty much any other gene. In nature, there is also a wide range of female resistance to harm from males — as well as ample evidence that males do harm females, often reducing their fitness.

For example, in Drosophila, a common fruit fly and the geneticists' favorite subject, mating success of males is an important issue — the female flies store sperm, and often use stored sperm for fertilizing all of its eggs; however, future re-matings may change that — i.e., the female might use fresher sperm. If there's re-mating, then sperm from different males would compete with each other for fertilization. That led to the evolution of more and more potent sperm; it was shown in the laboratory that the increased potency of sperm can be evolved in the lab, and that the female flies evolve corresponding resistance. This 'supersperm' is potent enough to kill females who have not evolved the corresponding defenses.

In terms of progeny, this conflict becomes complicated — after all, we are the product of two parental genomes, which may be in conflict with each other. And this is where the idea of parental imprinting of genes (perhaps one of the most intriguing areas of genetic research) comes into play. "Imprinting" in this context means that the copies of some genes behave differently depending on which parental source they came from. For example, in female mammals only one X chromosome is active — in early embryonic development, it is the copy from the egg that is active in the embryo. Later on, the inactive paternal X is released, and then X chromosomes are inactivated randomly in different cells — this is how we get tortoiseshell and calico cats, each different color patch corresponding to the original cell in the embryo, indicating either paternal or maternal X chromosome being active. So all female mammals are in effect mosaics of their maternal and paternal X chromosomes.

Some diseases are also associated with parental imprinting — for example, both Prader-Willi and Angelman syndromes are associated with a deletion on chromosome 15. If the deletion originated in the egg, the individual will have Angelman syndrome, and if it originated in the sperm — Prader-Willi syndrome. In the rest of us, both copies are present, indicating that both paternal and maternal imprinting are necessary for normal development.

Besides delaying male obsolescence, imprinting has a number of fascinating genetic consequences — and one of them had recently (in the past ten years or so) has drawn quite a bit of scientific and lay attention, because it seemed to shed some harsh light on the most sacred and frequently romanticized of human relationships — the bond between mother and child.

Evolutionary biologists working with both plants and animals have noticed one interesting issue: a conflict between maternal interests and those of the developing embryo. It is clearly in the maternal interest to limit the nutrients she allocates to any given offspring in favor of her own health and survival as well as the any future offspring she might have. The embryo, on the other hand, would clearly benefit from the increase of maternal allocation.

The genes that increase embryo's ability to demand and receive more resources are imprinted by the father — especially in species where multiple paternities are likely (a good percentage of mammals). The natural selection is likely to favor the offspring of the males that are able to increase maternal allocation at the expense of both the mother and her future offspring. Thus, it results in many unsightly things happening in the mammalian womb: sib murder, as well as tapping of the maternal resources in the manner most similar to parasitism.

Search for genes responsible is well in progress. Mice, who are fairly similar to humans genetically, have a gene known as Mest. It is imprinted paternally, and it regulates maternal care. Mice who are missing this gene are shockingly bad mothers — they pretty much ignore their helpless progeny, usually resulting in their death.

A Mest gene was located in humans; however, it is unclear (and unlikely) that the gene would have such clear-cut consequences, since in humans parental behavior is the result of learning and socialization; moreover, any effects of such genes are likely to be masked by family and social support systems. Instead, in humans the conflict between the mother and offspring are more likely to play out in the womb.

In placental mammals, the embryo implants in the womb and the exchange of nutrients and chemical signals occurs across the placenta. According to David Haig, one of the world's leading authorities in the issue, there is quite a bit of evidence that the evolutionary arms race resulted in the embryo secreting a lot of hormones designed to manipulate the mother into increasing a nutrient output, while the mother shows very little response to these demands — such resistance likely to have evolved during the selection process as well. Ultimately, the mother and the embryo are two separate beings, honed by the evolutionary process for maximum self-interest, and mothers' resistance to the embryonic demands ensure her own survival as well as her ability to have more offspring in the future.

Incidentally, this conflict is likely the reason why pregnancy carries so many hazards for the mother — especially considering how common this process is. Most routine biological processes do not carry such a high risk of complications and mortality; the reason why pregnancy is so hazardous is the competing interests of the embryo who uses the placenta to invade and divert maternal blood supply, and to send chemical messages to manipulate the maternal investment and resource allocation.

Many of the genes that are expressed in placenta are, not surprisingly, also imprinted by the father. From the genetic perspective, the father and his offspring share common genes, while the father and the mother (and whatever other offspring she may have in the future) do not; as the result, the selective process would favor father's ability to increase the survival of his offspring at the expense of the mother and half-siblings.

But what about mother's genes? Since the offspring shares half of the genes with the mother, it would stand to reason that there would be some synchronization and common interest between mother's and offspring's behavior, increasing the survival of both. There are many such examples — such as offspring begging for food causes a maternal response of feeding (unlike the case of placenta where embryonic demands are pretty much ignored.) Such harmonious coevolved behaviors of offspring and mother are likely to be due to the maternal genes.

Each of us is the product of two parental genomes, which often have conflicting interests. These conflicts can play out in the offspring-mother conflict as seen in the expression of Mest and placental genes, as well as the wider issue of parental imprinting.

 

References used:

Dawkins, R. (1976) The Selfish Gene, Oxford: Oxford University Press

Genomic Imprinting: A Talk with David Haig (2002). Edge (www.edge.org)

Godfray, H. C. J. (2002) Evolutionary theory of parent—offspring conflict (review article). Nature 376: 133-138

Linder, J.E. and W.R Rice. (2005) Natural selection and genetic variation for female resistance to harm from males. Journal of Evolutionary Biology 18: 568—575

Panhuis, T.W., N.L. Clark, and W.J. Swanson (2006) Rapid evolution of reproductive proteins in abalone and Drosophila. Philosophical Transactions of the Royal Society of London: Biological Sciences 361: 261—268.

Wade, N. (1998) Good Maternal Behavior Is Linked to the Genes of a Father. New York Times, 29 September. [Online] http://query.nytimes.com/gst/fullpage.html?sec=health&res=
9E0CE1DA1039F93AA1575AC0A96E958260
Retrieved 15 February 2008.

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ISSUE 18, March 2008

Outer Space
 

Helen Marshall
 

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ABOUT THE AUTHOR

Ekaterina Sedia

Ekaterina Sedia resides in the Pinelands of New Jersey. Her critically-acclaimed and award-nominated novels, The Secret History of Moscow, The Alchemy of Stone, The House of Discarded Dreams, and Heart of Iron, were published by Prime Books. Her short stories have sold to Analog, Baen's Universe, Subterranean, and Clarkesworld, as well as numerous anthologies, including Haunted Legends and Magic in the Mirrorstone. She is also the editor of the anthologies Paper Cities (World Fantasy Award winner), Running with the Pack, and Bewere the Night, as well as forthcoming Bloody Fabulous and Wilful Impropriety. Her short-story collection, Moscow But Dreaming, will be released by Prime Books in December 2012.

WEBSITE

www.ekaterinasedia.com

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