In a patch of grass along the Gulf Coast, a Texas field cricket rubs his wings together to produce his characteristic "chirp." He's playing a courting song to attract the attention of a nearby female. His advances work and she approaches. After brushing each other with their antennae, the pair get down to business. The female mounts the male to receive a packet of sperm that he has released onto his abdomen, and that will pump sperm into her for the next half hour.
It all seems perfectly normal — for bug sex, anyway — but there's actually something amiss here. Our six-legged Romeo is sterile, and his partner will soon be infertile. Her innards will become swollen and blue, and she won't produce any eggs from their tryst. There's no bouncing baby crickets on the way, and no happy ending to this romance. Except, that is, for a particular virus that has encouraged these star-crossed lovers to mate.
The virus, known as IIV-6/CrIV, benefits from the cricket's copulation because it spreads through sexual contact. And what's more, the virus promoted that contact in the first place, according to a new study.
It's a brilliant bit of behavior modification, similar to strategies employed by other viruses and parasites that can only flourish if their hosts do certain things. Rabies makes its hosts more aggressive so the virus can be spread by bites. Hairworms turn their grasshopper hosts into suicide jumpers so they can get to water. Some wasps force spiders to build weird webs to support their cocoons. All of this is done via chemical warfare waged on the host's central nervous system. A little venom here, or a tweak in hormone levels there, and the brain and body are hijacked for the parasite's own ends.
Biologist Shelley Adamo came across it in her lab at Dalhousie University in Nova Scotia when some of the crickets she kept there stopped laying eggs. She dissected some of the crickets and found that their fat bodies — an organ that stores fats and produces proteins for the immune system — were bloated and had turned blue. A peek through a microscope revealed that the organs were full of hexagonal viral particles that had packed themselves into a crystalline shape, which gave the fat body an eerie blue sheen.
The fat body is the perfect headquarters for interfering with communication between the immune system and the nervous system, and for altering its host's behavior and physiology.
And that's just what the virus did. The infected crickets could forget any chance of being parents. Adamo found that the females all had fewer than ten eggs inside them, while some had none. In contrast, a healthy cricket can usually hold more than a hundred. The males still produced sperm, but the cells were either severely crippled or entirely immobile. This kind of "parasitic castration" can help viruses and parasites secure more of the host's bodily resources for themselves without killing the host or hurting its ability to attract mates.
Despite their reproductive shortcomings, the crickets still wanted to mate. In fact, the males seemed more eager to get it on than usual. When Adamo and her team paired the crickets up, healthy, uninfected males waited around 10 minutes before they started serenading a female. Ones that were sick with a bacterial infection waited around 13 minutes — they were clearly not in the mood. Males that were infected with IIV-6/CrIV, on the other hand, didn't slow down at all. They actually started the mating game faster, taking only about three minutes to get courting. Meanwhile, the females, whether they had the virus or not, all mounted the males and took their broken sperm in the same amount of time.
The researchers think that the accelerated mating is a behavioral change forced by the virus so that it can be transmitted from cricket to cricket. About half of the infected-uninfected pairings led to the virus being spread. In some cases, the virus didn't even need the crickets to have sex, and hopped host-to-host while the insects nuzzled antennae during courtship.
The virus has another trick up its sleeve. Mucking with the crickets' immune system not only speeds up their courtship, but also keeps them in good enough shape to attract a mate. Animals that are sick usually won't put much, or any, effort into mating. They'll also often stop eating and lose weight while their immune systems fight off the infection. Other animals will pick up on these signs and avoid mating with sick suitors. That would be a dead end for a sexually transmitted infection, but the crickets with IIV-6/CrIV didn't show any of these "sickness behaviors" and were still attractive enough get other crickets to mate. They maintained their weight and went about their day as normal, the researchers think, because the virus keeps their fat bodies from producing the immune signals that tell them to do otherwise.
Adamo and her team aren't sure how IIV-6/CrIV does any of this, but they think it is at least partly attributable to a reduction in the host's overall protein content and the activity of virucidal enzymes. That would explain the lack of sickness behaviors, but not the males' speedy courting. Researchers will need to observe some more poor crickets mating futilely to fully understand the virus' exploitation of cricket sex.
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