4.4 Article

X-linked meiotic drive can boost population size and persistence

Journal

GENETICS
Volume 217, Issue 1, Pages -

Publisher

OXFORD UNIV PRESS INC
DOI: 10.1093/genetics/iyaa018

Keywords

sex ratio; selfish genetic elements; sex chromosome; levels of selection; polyandry; segregation distortion; eco-evolutionary model

Funding

  1. CoMPLEX Engineering and Physical Sciences Research Council [EP/N509577/1]
  2. Engineering and Physical Sciences Research Council [EP/F500351/1, EP/I017909/1]
  3. Natural Environment Research Council [NE/R010579/1]
  4. Biotechnology and Biological Sciences Research Council [BB/M011585/1, BB/P024726/1]
  5. Leverhulme Trust Early Career Fellowship [ECF-2020-095]
  6. EPSRC [EP/K038656/1, 2107972] Funding Source: UKRI
  7. NERC [NE/R010579/1] Funding Source: UKRI

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X-linked meiotic drivers can lead to an imbalance in sex ratios by producing an excess of X-bearing sperm in male carriers. The spread and fixation of X-linked alleles depend on sex-specific selection and transmission, rather than time spent in each sex. These drivers can enhance population size and persistence by increasing productivity, but can also lead to population extinction if the sex ratio becomes too skewed.
X-linked meiotic drivers cause X-bearing sperm to be produced in excess by male carriers, leading to female-biased sex ratios. Here, we find general conditions for the spread and fixation of X-linked alleles. Our conditions show that the spread of X-linked alleles depends on sex-specific selection and transmission rather than the time spent in each sex. Applying this logic to meiotic drive, we show that polymorphism is heavily dependent on sperm competition induced both by female and male mating behavior and the degree of compensation to gamete loss in the ejaculate size of drive males. We extend these evolutionary models to investigate the demographic consequences of biased sex ratios. Our results suggest driving X-alleles that invade and reach polymorphism (or fix and do not bias segregation excessively) will boost population size and persistence time by increasing population productivity, demonstrating the potential for selfish genetic elements to move sex ratios closer to the population-level optimum. However, when the spread of drive causes strong sex-ratio bias, it can lead to populations with so few males that females remain unmated, cannot produce offspring, and go extinct. This outcome is exacerbated when the male mating rate is low. We suggest that researchers should consider the potential for ecologically beneficial side effects of selfish genetic elements, especially in light of proposals to use meiotic drive for biological control.

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