Killer Chromosomes

There’s a killer lurking in the woods of North America, hiding in a place you would never suspect: the testes of a tiny fruit fly called Drosophila neotestacea. The testes are where sperm are produced, and each developing sperm cell contains exactly half the number of chromosomes as the father. This killer is chromosome, and so is its victim.

Fruit flies – like humans – have X and Y sex chromosomes. Females have two X-chromosomes, and males have one X and one Y-chromosome. This means that half of the sperm a male fly produces carry an X-chromosome, and the other half carry a Y-chromosome. When the sperm fuses with an egg from the mother during fertilization, whether a daughter or son is produced depends on whether the sperm has an X or a Y-chromosome. Typically, a father has an equal number of daughters and sons because he produces an equal number of X and Y-bearing sperm.

The killer X-chromosome in this species was discovered by accident in Dr. James Jaenike’s lab at the University of Rochester [1]. Certain male flies from a wild-caught sample produced only daughters when mated to lab females. Further investigation of this strange departure from the expected equal number of sons and daughters showed that through some unknown mechanism, the X-chromosome that these males carried was selfishly promoting its own transmission to the next generation by killing sperm that carried the Y-chromosome. Such selfish X-chromosomes – which are actually common in flies – are called sex-ratio X-chromosomes after the highly skewed offspring sex ratio they produce [2].

Theoretically, the killer sex-ratio X-chromosome is very bad for a population of flies because as it becomes more common, the population will contain many more females than males. If there aren’t enough males to fertilize all the females, too few offspring will be produced and the population will disappear completely [3]. But when flies in the wild were surveyed for the presence of the sex-ratio X-chromosome, in some places it was found at high frequencies – up to 40% of all X-chromosomes were sex-ratio X-chromosomes [4]! Even more surprisingly, repeated sampling across decades revealed that these frequencies are stable [4, 5]. There must be some other factor preventing the spread of the sex-ratio chromosome, and the key to identifying it lies in comparing populations that have very high frequencies of the sex-ratio chromosome with those that have very low frequencies of the sex-ratio chromosome. What factors differ between these populations that could counteract the selfish advantage of the sex-ratio X-chromosome?

Dr. Cheryl Pinzone addressed this problem in her dissertation research in Dr. Kelly Dyer’s lab at the University of Georgia by looking at female mating rate in populations of D. neotestacea [4]. The number of times that a female fly mates in the wild has the potential to affect sex-ratio X-chromosome frequencies. Because the action of the killer X-chromosome destroys all Y-bearing sperm, males carrying sex-ratio have half the amount of sperm that other males do. If females mate at an extremely high rate, then sex-ratio males could run out of sperm first, and sire less offspring overall than regular males. This limitation could negate the selfish advantage the sex-ratio X-chromosome has and keep it from overrunning the population. In order to test this idea, wild females were collected from multiple populations with different frequencies of sex-ratio, and the level of female mating and remating was determined in the lab. Overall, females from populations with low frequencies of sex-ratio mated more often and were more likely to remate than females from populations with high frequencies of sex-ratio. This data suggests that female mating behavior could be an important factor in keeping Drosophila neotestacea’s killer X-chromosome from going on a rampage.

  1. James, A.C. and J. Jaenike, Sex-ratio meiotic drive in Drosophila-testacea. Genetics, 1990. 126(3): p. 651-656.
  2. Jaenike, J., Sex chromosome meiotic drive. Annual Review of Ecology and Systematics, 2001. 32: p. 25-49.
  3. Hamilton, W.D., Extraordinary sex ratios. A sex-ratio theory for sex linkage and inbreeding has new implications in cytogenetics and entomology. Science, 1967. 156(3774): p. 477-88.
  4. Pinzone, C.A. and K.A. Dyer, Association of polyandry and sex-ratio drive prevalence in natural populations of Drosophila neotestacea. Proceedings. Biological sciences / The Royal Society, 2013. 280(1769): p. 20131397.
  5. Dyer, K.A., Local selection underlies the geographic distribution of sex-ratio drive in Drosophila neotestacea. Evolution; international journal of organic evolution, 2012. 66(4): p. 973-84.

katiepieper

Katie Pieper is a PhD student in the Department of Genetics at the UGA. She studies the molecular evolution of sex chromosomes in fruit flies. In her free time, she enjoys baking delicious desserts and winning at trivia contests. She is also the head tweeter for the Athens Science Café official Twitter account (@athscicaf). Get in touch with Katie at @kpeeps111 or kpieper@uga.edu