Gender-specific fitness?

Study finds that reproductively successful males have unsuccessful daughters

By | June 27, 2007

Genes that are advantageous to males may hinder fitness in females of the same species, according to a study of wild red deer in this week's Nature. The authors found that reproductively successful males had female relatives that reproduced less than average. Conflicting selection between the sexes may preserve trait diversity in the wild, the authors say. This work "is the first to provide compelling evidence of sexually antagonistic fitness variation in a wild population," said Russell Bonduriansky of the University of New South Wales in Sydney, Australia, who was not involved in the work. It should "dispel any lingering doubts about the reality and importance" of sex-specific selection, he added. Previous work has shown that genes are selected differently in females and males of laboratory organisms such as Drosophila melanogaster and the plant Silene latifolia. "The Drosophila studies were very powerful in terms of the genetic tools and ability to conduct highly controlled manipulations," Bonduriansky told The Scientist in an Email. "But these studies were also open to the criticism that the animals themselves were 'unnatural'" because they were laboratory-raised flies. Foerster and her colleagues analyzed data collected between 1971 and 2005 from a population of Cervus elaphus deer in Scotland. They measured the fitness of individual animals with a method that estimates each animal's contribution to population growth through both survival and reproduction. The authors found that male deer with relatively high fitness over their lifetimes tended to have daughters with relatively low fitness. Using an alternative statistical approach, they also found that male deer that sired the most offspring had female relatives with fewer calves, while male deer with fewer offspring had female relatives with more offspring. "There is a trade-off between optimal genes for males and for females of a species," first author Katharina Foerster of the University of Edinburgh, UK, told The Scientist in an Email. "Good genes may often be context-specific." The researchers did not find that highly fit females had less fit sons, however. This may result from mothers' influence on their offspring through early-life care, according to Foerster. Female deer "care for both sons and daughters similarly, and this may compensate for any genetic disadvantages" sons may have, she said. Bonduriansky said he's "not completely convinced by the explanation" that maternal care equalizes fitness of male offspring. However, he added, "this is just one of many interesting avenues for further investigation suggested by this study." The authors also found no relationship between fitness of male deer and their male offspring. They speculate that fathers cannot pass on these traits to their sons because sexually antagonistic genes are located on the X chromosome. "This is very likely for sexually antagonistic effects," Foerster said. Previous work discovered X-linked sexually antagonistic genes in Drosophila. It's not easy to study sexual differences in gene selection, said Adam Chippindale of Queen's University in Kingston, Canada. "Even in the lab, these kinds of data are always going to be difficult to generate," he said. In the current study, "they've done this long and arduous experiment, watching these deer for decades, and the results are brilliant," Chippindale told The Scientist. "It's extremely hard to measure fitness in the first place, let alone transmission of fitness from one generation to the next and in both sexes." If more good data can be collected, researchers will likely find that sex-specific gene selection is "ubiquitous in sexual organisms, because the two sexes have different fitness agendas," Chippindale added. "Good genes are only good if they're in the right sexual environment." Melissa Lee Phillips mail@the-scientist.com Links within this article K. Foerster et al., "Sexually antagonistic genetic variation for fitness in red deer," Nature, June 28, 2007. http://www.nature.com/nature T. Toma, "Sex wars drive evolution," The Scientist, June 26, 2003. http://www.the-scientist.com/article/display/21410 Russell Bonduriansky http://www.bonduriansky.net/index.htm G. Flores, "Sexual conflict opposes sexual selection," The Scientist, October 24, 2006. http://www.the-scientist.com/news/display/25282/ A.K. Chippindale et al., "Negative genetic correlation for adult fitness between sexes reveals ontogenetic conflict in Drosophila," PNAS, February 13, 2001. http://www.the-scientist.com/pubmed/11172009 T.R. Meagher, The quantitative genetics of sexual dimorphism in Silene latifolia (Caryophyllaceae). 1. Genetic variation," Evolution, 1992. http://links.jstor.org/sici?sici=0014-3820(199204)46:2%3C445:TQGOSD%3E2.0.CO;2-5 B. Borrell, "Origin of a controversy," The Scientist, January 1, 2007. http://www.the-scientist.com/article/display/39385/ Katharina Foerster http://homepages.ed.ac.uk/loeske/kathi.html J.R. Gibson et al., "The X chromosome is a hot spot for sexually antagonistic fitness variation," Proceedings of the Royal Society B, March 7, 2002. http://www.the-scientist.com/pubmed/11886642 Adam Chippindale http://www.achippindale.com/home.html
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