A Synthetic Maternal-Effect Selfish Genetic Element Drives Population Replacement in
            Drosophila

A number of species are affected by Sex-Ratio (SR) meiotic drive, a selfish genetic element located on the X-chromosome that causes dysfunction of Y-bearing sperm. SR is transmitted to up to 100% of offspring, causing extreme sex ratio bias. SR in several species is found in a stable polymorphism at a moderate frequency, suggesting there must be strong frequency-dependent selection resisting its spread. We investigate the effect of SR on female and male egg-to-adult viability in the Malaysian stalk-eyed fly, Teleopsis dalmanni . SR meiotic drive in this species is old, and appears to be broadly stable at a moderate (approx. 20%) frequency. We use large-scale controlled crosses to estimate the strength of selection acting against SR in female and male carriers. We find that SR reduces the egg-to-adult viability of both sexes. In females, homozygous females experience greater reduction in viability ( s f = 0.242) and the deleterious effects of SR are additive ( h = 0.511). The male deficit in viability ( s m = 0.214) is not different from that in homozygous females. The evidence does not support the expectation that deleterious side effects of SR are recessive or sex-limited. We discuss how these reductions in egg-to-adult survival, as well as other forms of selection acting on SR, may maintain the SR polymorphism in this species.

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Maternal effect killing by a supergene controlling ant social organization

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.2003282117 ◽

2020 ◽

Vol 117 (29) ◽

pp. 17130-17134

Author(s):

Amaury Avril ◽

Jessica Purcell ◽

Sébastien Béniguel ◽

Michel Chapuisat

Keyword(s):

Social Organization ◽

Maternal Effect ◽

Evolutionary Dynamics ◽

Mendelian Inheritance ◽

Transmission Ratio Distortion ◽

Gene Drive ◽

Biological Organization ◽

Evolutionary Mechanisms ◽

Selfish Gene ◽

Selfish Genetic Element

Supergenes underlie striking polymorphisms in nature, yet the evolutionary mechanisms by which they arise and persist remain enigmatic. These clusters of linked loci can spread in populations because they captured coadapted alleles or by selfishly distorting the laws of Mendelian inheritance. Here, we show that the supergene haplotype associated with multiple-queen colonies in Alpine silver ants is a maternal effect killer. All eggs from heterozygous queens failed to hatch when they did not inherit this haplotype. Hence, the haplotype specific to multiple-queen colonies is a selfish genetic element that enhances its own transmission by causing developmental arrest of progeny that do not carry it. At the population level, such transmission ratio distortion favors the spread of multiple-queen colonies, to the detriment of the alternative haplotype associated with single-queen colonies. Hence, selfish gene drive by one haplotype will impact the evolutionary dynamics of alternative forms of colony social organization. This killer hidden in a social supergene shows that large nonrecombining genomic regions are prone to cause multifarious effects across levels of biological organization.

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