Scrambling eggs toasts meiotic drive

Yaniv and I’s paper: “Scrambling eggs: Meiotic Drive and the Evolution of Female Recombination Rates” is out on the Genetics preprint server (here) and the arXived versions of our paper are available here.

Conflict is everywhere during sexual reproduction. Even meiosis is a battlefield (Pat Benatar had that right), as during meiosis and gametogenesis alleles can complete with each other within an individual to ensure their transmission to the next generation. No where is this more apparent than during female meiosis, where out of the 4 products of meiosis only one will go on to form the egg. This allows an opportunity for (true) meiotic drive, as an allele that distort meiosis in its favor when heterozygous can spread through the population. One great example of female meiotic drive is the chromosome knob system in maize (see here and references within), another putative example is provided by the great work of Fishman and Willis in Mimulus (here and here). There’s even female meiotic drive alleles humans, by chromosomal fusions, but the deleterious consequences in males mean that they only persist for short time periods.

Such selfish drive systems set up the arena for further conflict, especially if they have deleterious consequences. Alleles that facilitate this drive can also spread if they team up with the meiotic drive alleles. While alleles that suppress the drive can spread as they benefit from the reduced transmission of the deleterious driver to their descendents.

In our latest paper, Yaniv and I explore how models of meiotic drive may have shaped sex differences in recombination rates. In many systems recombination is an essential part of meiosis, with at least one crossover required per chromosome to ensure correct segregation. Perhaps surprisingly then recombination rates evolve very rapidly and the sexes often differ dramatically in their number of recombination events and their positions. For example in humans ~26 events are placed down during male meiosis but around 40 are placed down in female meiosis. This pattern of sex differences in recombination rates is wide-spread, with female recombination rates often -but not always- being higher than male rates. Yaniv and I suggest that this could be due to the role of female recombination in facilitating or ameliorating female meiotic drive. The details are a bit involved, as the predictions vary depending on which stage of meiosis drive alleles take advantage of. But the basic idea is that because the centromere plays such a key role in meiosis and recombination determines whether alleles segregate with their, or their non-sister centromere, changes to the female recombination can have powerful effects on meiotic drive and be selected on as a consequence.

We see this work as part of the emerging picture that conflict may be common in meiosis and that various features of meiosis, from the complexity of centromeres, to the stages of meiosis, to sex itself may have been profoundly shaped by this struggle (Burt and Trivers’s book is a great place to read about this). These ideas has been around for a long time and have a lot to recommend them, indeed the idea that drive may affect recombination rates has been around for a while (see Thomson and Feldman, Haig and Grafen), however, the sex-specific context had received little attention (but see Haig 2010, and Lenormand 2003). Strangely these conflict ideas are often ignored by researchers interested in recombination and its evolution, who seem to prefer to focus on more traditional explanations for sex and recombination due to recombination role in facilitating or hindering selection.

The rapid evolution of many components of meiosis is certainly consistent with these types of conflict hypotheses, and our own work on PRDM9 suggests that even the fine-scale features of recombination may be involved in another facet of these types of conflict. We have a long way to go in understanding the causes and consequences of these conflicts, but hopefully advances in sequencing technology will allow us to investigate distortion and recombination in meiosis in fuller detail.

[UPDATED: Thanks to Jeff Ross-Ibarra for edits]

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4 Responses to Scrambling eggs toasts meiotic drive

  1. Why female rather than male though? And why is female recombination higher than the male recombination? Looking forward to reading the paper – I have always been curious about Drosophila males refusing to recombine at all.

    • cooplab says:

      Hi Dmitri,
      Our model has a variety of predictions, as linked and unlinked recom. modifiers, and MI and MII drive lead to different predictions. So it is hard to make specific predictions. However, to make a post hoc story, the generally higher rates in females, under our model, is consist with frequent MI drive being suppressed by females cranking up their recom rates. We lay this out more in the article. The absence of recom in D. males is an example of the Haldane-Huxley rule, and is likely a different phenomenon.

      Graham

  2. cooplab says:

    An extra note, so it’s helpful to distinguish two cases:
    1) When recombination is absent from one sex, and the sex chr. are heteromorphic, then it’s nearly always the heterogametic sex that lacks crossing over. There’s >35 independent cases of this. This is the Haldane-Huxley rule, there are very few exceptions. This is probably because you can’t be XY in a system with no recom in females, as you’d soon lose your X as well. There’s some support for that idea, that I keep meaning to write up.

    2) When both sexes recombine, females often-but not always-have higher recombination rates, regardless of which sex is heterogametic. See our figure 1 and Lenormand’s 2005 PLoS Bio. paper. It’s this second form of sex-differences that our article sets out to explain.

  3. Pingback: Scambling eggs toasts meiotic drive out in Genetics | gcbias

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