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Why Sex? Now Shown That in Water Fleas, Recombination Does Lead to Fewer Deleterious Mutations

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Why Sex? Now Shown That in Water Fleas, Recombination Does Lead to Fewer Deleterious Mutations PERSPECTIVES EVOLUTION It is assumed that most organisms have sex because the resulting genetic recombination allows Darwinian selection to work better. It is Why Sex? now shown that in water fleas, recombination does lead to fewer deleterious mutations. Rasmus Nielsen hy sex? This has been one of the most sexual reproduction. Additionally, fundamental questions in evolution- the best explanations regarding dele- Wary biology. In many species, males terious mutations rely on strong do not provide parental care to the offspring. assumptions regarding the distribu- Clearly, the rate of reproduction could be tion of selective effects (3), and there increased if all individuals were born as females may be other factors favoring and reproduced asexually without the need to sex, such as increased resistance to mate with a male (parthenogenetic reproduc- pathogens (4). An observed genomic tion). Parthenogenetically reproducing females correlation between the rate of recom- arising in a sexual population should have a bination and variability within species twofold fitness advantage because they, on aver- (5) suggests that there is an interaction age, leave twice as many gene copies in the next between selection and recombination, generation. Nonetheless, sexual reproduction is but a direct difference between sexual ubiquitous in higher organisms. Why do all these and asexual populations has been hard species bother to have males, if males are associ- to establish. ated with a reduction in fitness? The main solu- However, the new study by Paland tion that population geneticists have proposed to and Lynch (1) provides direct empir- this conundrum is that sexual reproduction ical support for an excess accumula- allows genetic recombination, and that genetic tion of mutations in asexually repro- recombination is advantageous because it allows ducing populations compared to natural Darwinian selection to work more effi- sexual populations. They examined ciently. New empirical evidence supporting this different populations of the small theory now comes from a study by Paland and crustacean Daphnia pulex, a type of Lynch on page 990 in this issue (1). water flea. Daphnia are excellent One reason why selection works more effi- organisms to study in this regard ciently in the presence of recombination—that because parthenogenetic Daphnia is, the exchange of genetic material between populations have arisen multiple chromosomes—is that selected mutations tend times from sexual populations. Com- to interfere with each other in the absence of paring asexual and sexual popula- recombination (2, 3). Imagine, for example, a tions of Daphnia is, therefore, the beneficial mutation (A) arising in one individual perfect tool for examining the popu- and another beneficial mutation (B) arising in lation genetic consequences of another gene in an individual that does not carry Lessons from the flea. The water flea, Daphnia pulex, may shift sexual reproduction (see the figure). mutation A. In the absence of recombination, from being sexual to being asexual and is, therefore, an excellent Paland and Lynch (1) compared mutation B would be eliminated when mutation research tool for testing theories regarding the evolution of sex- the number of mutations with possi- A reaches a frequency of 100% in the popula- ual reproduction. The drawing [from (9)] is by J. J. Paschoud in ble functional effects (nonsynony- tion, and vice versa. No individual carrying both the late 1700s. mous mutations) to the number of beneficial mutations could be created, and only mutations with no functional effects one of the mutations could eventually reach a but if you can replace the broken part in one car (synonymous mutations) in 14 asexual and 14 frequency of one in the population. Recom- with a part from the other car you can produce a sexual Daphnia populations. They observed a bination speeds up the rate of adaptive evolu- new functional car. Recombination allows bro- clear excess of nonsynonymous mutations in the tion because it allows several beneficial muta- ken parts to be shuffled among chromosomes, asexual populations. They also estimated that tions to be combined in the same individual. allowing new combinations to arise for selec- close to 90% of the nonsynonymous mutations Likewise, when multiple deleterious mutations tion to act on. Under suitable assumptions were subject to selection. These results suggest are present in the population, recombination regarding the way deleterious mutations affect that the asexually reproducing species carry a has the potential for creating new offspring organismal fitness, the advantage of recombi- higher load of deleterious mutations and that chromosomes with fewer deleterious mutations nation in eliminating deleterious mutations can selection is not as efficient in the asexual as than either of the parental chromosomes. The outweigh the twofold cost of sex (3). in the sexual populations. It does not directly famous population geneticist John Maynard- However, the selection theories are not free demonstrate that selection against deleterious Smith compared this situation to having two of contradictions and problems. Some of them mutations is what maintains sexual reproduc- cars: one with a broken engine and one with a rely on so-called group-selection arguments, tion, but the results do confirm the most broken transmission. Neither of them can run, where adaptive properties are properties of a important component of the selection theory: whole population and not of individuals. If sexu- Asexual reproduction leads to an accumulation ally reproducing individuals and their offspring of deleterious mutations. It seems that males The author is at the Center for Bioinformatics and Department of Biology, University of Copenhagen, do not have an immediate selective advantage in are allowed to exist after all, because they help Universitetsparken 15, 2100 Kbh Ø Denmark. E-mail: otherwise asexual populations, it is hard to see females get rid of deleterious mutations. [email protected] how populations can ever evolve from asexual to The study is also interesting from another 960 17 FEBRUARY 2006 VOL 311 SCIENCE www.sciencemag.org Published by AAAS PERSPECTIVES point of view. The estimate of the proportion of schauung in evolutionary biology is changing 3. A. S. Kondrashov, Nature 336, 435 (1988). new mutations in Daphnia that are under selec- from a static view of a largely optimized 4. W. D. Hamilton et al,. Proc. Natl. Acad. Sci. U.S.A. 87, 3566 (1990). tion is fairly high (>90%). Over the past 30 genome to a dynamic view of organisms con- 5. D. J. Begun, C. F. Aquadro, Nature 356, 519 (1992). years, the paradigmatic theory in molecular evo- stantly challenged by selection and struggling 6. M. Kimura, The Neutral Theory of Molecular Evolution lution has been the Neutral Theory (6), which with the large genetic load imposed by deleteri- (Cambridge Univ. Press, Cambridge, UK, 1983). assumes that the vast majority of genetic poly- ous and new advantageous mutations segregat- 7. S. Williamson et al., Proc. Natl. Acad. Sci. U.S.A. 102, 7882 (2005). morphisms have little or no selection acting ing in the population. 8. P. Andolfatto, Nature 437, 1149 (2005). upon them. However, the study by Paland and 9. L. Jurine, Histoire des Monocles, qui se Trouvent aux Lynch (1), and other recent studies (7, 8), sug- References Environs de Geneve (Paris, 1820). 1. S. Paland, M. Lynch, Science 311, 990 (2006). gest instead that many or most polymorphisms 2. J. Maynard-Smith, The Evolution of Sex (Cambridge Univ. may be under selection. Slowly, our weltan- Press, Cambridge, UK, 1978). 10.1126/science.1124663 PLANETARY SCIENCE The Hubble Space Telescope has revealed two new moons and two new rings orbiting Uranus. Ringing the Changes The images indicate a dynamic, evolving, and possibly unstable ring system. Carl D. Murray t all seemed so simple for a while. As far as ture is not yet complete. Observations of small the surface of the moon, they still have orbital we knew, Jupiter, Saturn, Uranus, and moons this close to a planet are notoriously dif- energies comparable to their parent body and so INeptune each had a ring system, a suite of ficult; long exposures are required, and the remain in a broadly similar orbit. Jupiter, Saturn, small moons orbiting just beyond or close to brightness of the planet tends to result in pic- and Neptune all have examples of small moons the rings, followed by an impressive set of tures with extensive “bloom” where saturated embedded in faint rings. There are still some large moons and finally an irregular collection detector pixels engulf the image. However, by anomalies in Mab’s orbit that need to be under- of outer moons in eccentric, inclined orbits. making use of the fact that the bloom on stood, but the association with R1 seems clear. But now Uranus has yielded a few more secrets Hubble’s High Resolution Camera is always in The Hubble observations have also shown that in the form of new moons and new rings. The the vertical direction, the authors were able to Puck, which orbits at the inner edge of R1, moons may be tiny and the rings faint, but the align and time their images such that all the appears to have one side that is 10% brighter research reported by Showalter and Lissauer inner moons would show up in sufficiently long than the other. Puck, like our own and many (1) on page 973 of this issue reveals a compli- exposures. This led to the discovery of two new other moons, is tidally locked to its planet and cated, evolving system that provides a fascinat- moons, Cupid and Mab, and two faint, diffuse therefore has well-defined leading and trailing ing insight into how rings and small moons are rings that they refer to as R1 and R2. hemispheres. Given that it is Puck’s trailing side inextricably linked. The outer ring, R1, peaks in intensity at the that is brighter, the clear implication is that Of all the ringed planets, Uranus’s ring sys- orbit of Mab.
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