Antagonistic pleiotropy hypothesis

Antagonistic pleiotropy hypothesis

The antagonistic pleiotropy hypothesis was first proposed by George C. Williams in 1957 as an explanation for senescence. [Williams, G.C. 1957. Pleiotropy, natural selection, and the evolution of senescence. Evolution 11:398–411.] Pleiotropy is the phenomenon where one gene controls for more than one phenotypic trait in an organism. [ Cheverud, J. 1996. Developmental integration and the evolution of pleiotropy. American Zoology 36:44-50.] Antagonistic Pleiotropy is when one gene controls for more than one trait where at least one of these traits is beneficial to the organism's fitness and at least one is detrimental to the organism's fitness [Elena, S.F. and R. Sanjuán. 2003. Climb every mountain? Science 302:5653:2074-2075] The theme of G.C. William's idea about antagonistic pleiotropy was that if a gene caused both increased reproduction in early life and aging in later life, then senescence would be adaptive in evolution. For example, one study suggests that since follicular depletion in human females causes both more regular cycles in early life and loss of fertility later in life through menopause, it can be selected for by having its early benefits outweigh its late costs. [ Wood, J.W., K.A. O'Conner, D.J. Holman, E. Bringle, S.H. Barsom, M.A. Grimes. 2001. The evolution of menopause by antagonistic pleiotropy. Center for Demography and Ecology, Working Paper. ]

As a constraint on perfection

Antagonistic pleiotropy is one of the several reasons evolutionary biologists give for organisms never being able to reach perfection through natural selection. Antagonistically pleiotropic genes are the explanation for fitness trade-offs. [Elena, S.F. and R. Sanjuán. 2003. Climb every mountain? Science 302:5653:2074-2075] This means that genes that are pleiotropic and control for some beneficial traits and some detrimental traits; thus, if they happen to persist through natural selection, this will prevent organisms from reaching perfection because if they possess the benefits of the gene, they must also possess the imperfections or faults. An example of this would be female rodents that live in a nest with other females and young may end up feeding young that are not theirs due to their intense parental drive. [Alcock, J. 2005. Animal Behavior: eighth edition] This strong parental drive will be selected for, but the organisms will still make the mistake of feeding young that are not theirs and mis-allocating their resources.

Benefits and costs

Antagonistic Pleiotropy has several negative consequences. It results in delayed adaptation, an altered path of evolution, and reduced adaptation of other traits. [Otto, S.P. 2004. Two steps forward, one step back: the pleiotropic effects of favoured alleles.] In addition, The overall benefit of alleles is cut down significantly (by about half) by pleiotropy. Still, Antagonistic Pleiotropy has some evolutionary benefits. In fact, The conservation of genes is directly related to the pleiotropic character of an organism. [He, X. and J. Zhang. 2006. Toward a Molecular Understanding of Pleiotropy. Genetics 173:1885-1891] This implies that genes that control for multiple traits, even if the traits have different implications for the organism's fitness, have more staying power in an evolutionary context.

Antagonistic pleiotropy is ubiquitous

Although there are so many negative effects related to genes that are antagonistically pleiotropic, it is still present among most forms of life. Indeed, pleiotropy is one of the most common traits possessed by genes overall. [He, X. and J. Zhang. 2006. Toward a Molecular Understanding of Pleiotropy. Genetics 173:1885-1891] In addition to that, pleiotropy is under strong stabilizing selection. [Otto, S.P. 2004. Two steps forward, one step back: the pleiotropic effects of favoured alleles. Proc. Biol. Sci. 271:1540:705-714.] In one experiment with mice and the morphology of the mandible, 1/5 of the loci had effects of pleiotropy for the entire mandible. [Cheverud, J. 1996. Developmental integration and the evolution of pleiotropy. American Zoology 36:44-50.] One other example was in the Russian biologist Dmitry K. Belyaev's study on the domestication of the fox. [Trut, L.N. 1996. Early canid domestication: the farm-fox experiment. American Scientist 87:2:160-159.] In Dmitry K. Belyaev's farm-fox experiment, wild foxes were bred for docile behavior alone. After 40 generations, other physiological changes had surfaced including shortened tails, floppy ears, a white star in the forehead, rolled tails, shorter legs. Since the only thing being selected for was behavior, this leads scientists to believe that these secondary characteristics were controlled by the same gene or genes as docile behavior.

Adaptivity and senescence

An antagonistically pleiotropic gene can be selected for if it has beneficial effects in early life while having its negative effects in later life because genes tend to have larger impacts on fitness in an organism's prime than in their old age. [Wood, J.W., K.A. O'Conner, D.J. Holman, E. Bringle, S.H. Barsom, M.A. Grimes. 2001. The evolution of menopause by antagonistic pleiotropy. Center for Demography and Ecology, Working Paper.] An example of this is testosterone levels in male humans. Higher levels of this hormone lead to increased fitness in early life, while causing decreased fitness in later life due to a higher risk for prostate cancer. [Gann, P.H., C.H. Hennekens, J. Ma, C. Longcope, M.J. Stampfer. 1996. Prospective Study of Sex Hormone Levels and Risk of Prostate Cancer. Journal of the National Cancer Institute 88:16:1118-1126.] This is an example of antagonistic pleiotropy being an explanation for senescence. Senescence is the act of ageing in individuals; it's the failure over time of the individual's life processes by natural causes. [Promislow, D.E.L. 2004. Protein networks, pleiotropy and the evolution of senescence. Proc. Biol. Sci. 271:1545:1225-1234.] Williams's theory has been the motivation for many of the experimental studies on the reasons for aging in the last 25 years. [Fox, C.W. and J.B. Wolf. 2006. Evolutionary Genetics: Concepts and Case Studies.] However there is more than one theory out there for aging. The competing model to explain senescence is Medawar's "mutation accumulation" hypothesis, saying that "over evolutionary time, late-acting mutations will accumulate at a much faster rate than early-acting mutation. These late-acting mutations will thus lead to declining viability and/or fertility as an organism ages." [Fox, C.W. and J.B. Wolf. 2006. Evolutionary Genetics: Concepts and Case Studies.]

References


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