Left: Green rice leafhopper (Nephotettix cincticeps); Right: Sperm heads showing DNA (blue) and Rickettsia (red). Credit: Watanabe et al, 2014
Left: Green rice leafhopper (Nephotettix cincticeps); Right: Sperm heads showing DNA (blue) and Rickettsia (red). Credit: Watanabe et al, 2014

Bug Inherits Microbes From Dad’s Sperm

The green rice leafhopper is never alone. When a female’s egg and a male’s sperm fuse into a new cell, that cell is already infected with bacteria. As the newly conceived leafhopper grows from one cell into millions, its internal bacteria—its endosymbionts—go along for the ride. Right from the start, the leafhopper isn’t an individual in its own right, but a collection of animal and microbes that live together.

Many insects and other animals inherit endosymbionts from their parents, but almost all of them do so from their mothers. There’s good reason for this. An egg cell is big. Its central nucleus, which contains its DNA, is surrounded by a spacious and roomy cytoplasm, which can house lots of bacteria. But a sperm cell has no cytoplasm, and its tiny head is all nucleus. This streamlined shape is good for swimming, but it’s terrible for packaging bacterial heirlooms. That’s why males almost never pass on endosymbionts to their kids, while females often do. Sperm just isn’t very good packing material.

But try telling that to the green rice leafhopper. This small green bug is a serious pests of rice plants in East Asia, and its cells are filled with at least three species of bacteria. And one of them—Rickettsia—can infect the insect’s sperm.

Kenji Watanabe and Hiroaki Noda from the National Institute of Agrobiological Sciences in Japan found that almost every one of the leafhopper’s sperm cells contains several copies of Rickettsia, with up to 23 microbes per head. The team have no idea how the bacteria gain entry, or why their presence doesn’t seem to harm or disable the sperm in any way. But they do know that if these infected sperm fertilise eggs, they can pass their copies of Rickettsia into the next generation.

This unique ability to transmit microbes via sperm could completely change the usual relationship between the insects and the bacteria. These partnerships are fairly straightforward if microbes are only passed down the maternal line. Every individual inherits a single strain of microbe, and they co-evolve in neat tandem. Buchnera, for example, lives inside the cells of aphids, and has been co-evolving with them for over 150 million years. If you draw the family tree of Buchnera strains, it would look almost identical to the family tree of their aphid hosts.

But in the leafhopper, both males and females can pass Rickettsia to their offspring, so each individual could end up with different bacterial strains. “Co-infections are likely to introduce more conflict with the host” as strains compete with each other, says Nancy Moran from the University of Texas in Austin. Conflicts between harmless bacteria can potentially harm their hosts, as the adaptations that allow one microbe to best another can sometimes allow them to cause disease. If that’s true here, Rickettsia may flip from being a harmless (or even beneficial) partner into an enemy.

Passing microbes through sperm also changes the battle of the sexes. Some endosymbionts are actively hostile to males since they can only spread via eggs and not sperm. The bacterium Wolbachia can sometimes kill males before they’re born, or convert them into females. It can force females to reproduce by cloning themselves, making males completely redundant. It sometimes uses a subtler trick called “cytoplasmic incompatibility“, where uninfected females cannot mate successfully with infected males. This means that infected females, who can mate with whomever they like, enjoy a big advantage over uninfected females, who are more restricted.

But these anti-male strategies would be less useful to an endosymbiont that can pass through sperm as well as eggs, like Rickettsia does. Watanabe and Noda found some evidence for this: they showed that infected males and uninfected females produce slightly fewer young that any other combination of partners. That looks a lot like cytoplasmic incompatibility, but it’s very mild compared to what Wolbachia does.

Jack Werren from Rochester University, who studies Wolbachia, says that the Japanese team found irrefutable evidence for sperm transmission, but their study also raises many questions. How does Rickettsia function inside the nucleus? And with its host’s DNA within easy reach, could it be manipulating the leafhopper’s genes?

And what’s Rickettsia doing inside its host? Is it a benign parasite, or is it actually helpful? Many endosymbionts provide their hosts with nutrients or defend them against parasites and diseases. Aphids, for example, cannot survive without Buchnera. Rickettsia, however, seems to be dispensable. When Watanabe and Noda cured the leafhoppers of their infections, the adult insects seemed fine.

But as Werren points out, the team only studied small numbers of the insects in their laboratory. It’s possible that Rickettsia might help the leafhoppers by protecting them from parasites, or even by detoxifying pesticides in their environment—benefits that would only reveal themselves in the wild.

Reference: Watanabe, Yukuhiro, Matsuura, Fukatsu & Noda. 2014. Intrasperm vertical symbiont transmission. PNAS http://dx.doi.org/10.1073/pnas.1402476111

Correction: The text originally identified Nancy Moran from the University of Texas in Austin as Nancy Dunbar from the University of Austin in Texas. Because I’m an idiot.