American Society of Naturalists

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“Maintenance of fertility in the face of meiotic drive”

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Lara Meade, Sam Finnegan, Ridhima Kad, Kevin Fowler, and Andrew Pomiankowski (Apr 2020)

Males with meiotic drive have enlarged testes to maintain high fertility despite the destruction of half their sperm

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Maintenance of fertility in the face of sperm destruction by meiotic drive

A male <i>Teleopsis dalmanni</i> stalk-eyed fly.<br/>(Credit: Kiran Lee, University College London)
A male Teleopsis dalmanni stalk-eyed fly.
(Credit: Kiran Lee, University College London)

Meiotic drive genes are selfish genetic elements that cause the destruction of sperm that do not carry the selfish gene. The consequent loss imposes a severe fertility disadvantage on males carrying the drive gene (“drive males”).

Dr. Lara Meade, Professor Andrew Pomiankowski and colleagues at University College London have uncovered an entirely novel response to meiotic drive. In the Malaysian stalk-eyed fly, Teleopsis dalmanni, X-linked meiotic drive causes the destruction of all Y-sperm. Surprisingly the fertility of males carrying the drive gene is not reduced. This is even the case when males are challenged to mate with large numbers of females over a short period of time. Drive and wildtype sperm delivery is identical. This highly unusual finding has a simple explanation. On dissection, the authors found that drive males have greatly enlarged testis size—the organ that produces sperm. Faced with sperm destruction, drive males compensate by increasing sperm production, bringing their fertility up to the level of wildtype males.

Increased testis size comes at a cost. Drive males have small eyespan—the highly sexually selected trait females use in their mate choice. Drive males also have small accessory glands—organs that produce essential components of the ejaculate. The authors suggest these patterns of trait development are connected. Small eyespan means drive males are unattractive and gain few mating opportunities. So, investment in accessory gland (which enables higher mating rates) gives a low return. It is better to divert resources into testis. This allows drive males to deliver sufficient sperm to compete under the conditions of high sperm competition seen in stalk-eyed flies.

Bizarrely, these responses to drive not only improve individual male fitness, but also intensify the transmission of the drive gene itself. The authors suggest that this may contribute to the persistence of this selfish gene in natural populations of stalk-eyed flies.


Abstract

Selfish genetic elements that gain a transmission advantage through the destruction of sperm have grave implications for drive male fertility. In the X-linked SR meiotic drive system of a stalk-eyed fly, we found that drive males have greatly enlarged testes and maintain high fertility despite the destruction of half their sperm, even when challenged with fertilizing large numbers of females. Conversely, we observed reduced allocation of resources to the accessory glands that probably explains the lower mating frequency of SR males. Body size and eyespan were also reduced, which are likely to impair viability and pre-copulatory success. We discuss the potential evolutionary causes of these differences between drive and standard males.