I am infested with parasites. My entire house is lousy with them—the word lousy is derived from the singular form for lice, a particular small mammalian ectoparasite. We categorize our parasites by where they live—the endoparasites like ascarid worms and nematodes, giardia, and strange things ingested in bad sushi live in our bowels. The ectoparasites (fleas, ticks, bedbugs, lice, etc.) expose themselves on our surface. They crawl in our pubic hair. They get us sent home from school with red faced parents who stop at the pharmacy for foul smelling shampoos and fine-toothed egg combs. 100% of humans tested at age 18 by Dr. Michelle Trautwein carry the ectoparasitic facial skin mite Demodex folliculorum or its close relative Demodex brevis. These mildly disgusting little arachnids live inside your hair follicles and sebaceous glands, respectively, and cause very little harm because this living space provides room for only a few milligrams of total parasitic load per human.
The hookworm is a good example of the typical endoparasite. Hookworms such as Necator americanus attach to the epithelial lining of the small intestine where they munch on the intestinal villae, cause bleeding, and then drink the leaking blood.
An 8 ounce load of intestinal hookworms is a severe infestation and will result in weight loss, anemia, malabsorption, and other overt symptoms of chronic illness. An amount of hookworms equal to the weight of a single house cat, perhaps 10 pounds, would eventually prove fatal. A link to a nice review of these conventional parasites (PDF) in human evolution was recently posted on Twitter by Jennifer Wagner @DNAlawyer. Like most modestly hygienic Americans, I have very small whole-body burdens of both exoparasites and endoparasites. But when it comes to social guest parasites, I’m suffering from an acute infestation.
Social parasitism is a unique parasitic niche, inhabited by creatures specifically adapted to exploit the complex living spaces, communication channels, and behaviors of social animals. While many species of animals form groups and have some social structure, highly social (eusocial) species are restricted to humans, ants, bees, termites, and wasps. (See E.O Wilson, The Insect Societies for many hours of reading about the latter four of those.) Entomologists have long studied the parasitic insects that live in close relationships with the social insects, as I will expand on below, and often give them the euphemistic name of guest. On further reading, one sees that they behave very badly as guests, if that is their status. Almost all of them end up consuming the eggs and young of their social insect host, which is fairly rude. I think “social guest parasite” is a more fitting term. Hosts usually mount some sort of immune or behavioral defense against their conventional parasites. The distinguishing feature of a social guest parasite is that the host actively coddles and protects it, most often mistaking it for its own kind.
The two main human social parasites are Felis silvestris catus the house cat, and Canis Canis the dog. I have the former. I am supporting at least 10 cats or about 120 pounds of parasites. This is not a survivable parasite load for any of the common intestinal worm infestations that I’ve taken care to avoid. Fortunately for me, my social guest parasites live on the couch, not in my bowels.
There is considerable argument whether the dog should be considered a human social symbiont or commensual and not a parasite, as the cat clearly is. Dogs work for humans and shoulder large labor burdens for them, as can be seen by Googling “Inuit sled dog” or “Irish border collie.” Cats, on the other hand, do not even listen to their human hosts, much less perform any chores for them. Dogs also are eaten as food in many cultures, making them livestock, while cats are not.* When humans keep, feed, and shelter a dog, the dog thinks the human is God and serves him faithfully. When humans keep, feed, and shelter a cat, the cat understands that it is God and expects the human to serve him faithfully. So we will leave dogs out of the current discussion as possibly still man’s best friend, and concentrate on cats, who are not.
Assisted by the spread of mankind, cats have extended their population from a small area of North Africa and the Middle East to the entire habitable area of the world. There are about 200 million of them in the US alone, evenly split between the parasitic niche (domesticated) and the feral state (in between hosts). An estimated $30 billion is spent each year by American hosts sustaining this parasite load of about 3 cat pounds per person. Even with the ever increasing cost of raising children, the amount of resources currently diverted to pet cats would raise an additional 3 million Americans to adulthood every year.
Our human social history is very short, but exactly how short is hard to say, as behaviors leave no fossils. Our entire genus goes back no more than 2.5 million years, and it is reasonable to think that when the human lineage split from that of chimps and bonobos, we had a rudimentary social system similar to theirs today. Chimps do not have pets; they do not have any affinity for cats or dogs, and so they have no guest parasites that exploit their sociality. Homo sapiens has been attended by guest parasites that exploit our unique and robust sociality for a very brief evolutionary interval, perhaps between 10,000 and 20,000 years. In that perspective, we are just seeing the nascent glimmerings (as in oncoming headlights) of the possible exploitation that is yet to come.
To get a better view of what can happen to hosts and guests locked in social parasitism, it is informative to look first at ants and termites. Their own sociality both predates ours by many tens of millions of years, and their social guest parasites are much more refined than our own. There are many forms of social parasitism in insects we can look at, including an advanced social parasite of ants, the Large Blue butterfly Phengaris arion.
The caterpillar hunches into a contorted posture while releasing pheromones. Together, the behavioral cue and chemical message informs the ant that it has found one of its own larvae, and it gently picks up the guest parasite and carries it back to the brood chamber of the ant colony. Here the butterfly larva slaughters and eats the ant brood while soliciting tropholaxis (demanding vomited food) from the nurse ants until it matures and undergoes pupation. Hatching of the adult butterfly completes the cycle.
The extremes to which evolution has selected features of guest parasite anatomy is exemplified by the termitophilous staphylinid beetles, guest parasites of African termites, shown below. The abdomen of the beetle has been distended and projected back over the dorsum of the insect, so that its anus sits directly above the head. Curious worker termites who approach the beetle actually interact with the anus and false appendages, rather than the actual head of the beetle hidden below. Pheromones secreted by perianal glands mimic those of worker termites. Exudatoria, or fake legs, dangle from the sides, making this a termite version of a human adult blow up doll. Following the lead of the Great Blue, staphylinid larvae become large consumers of termite eggs and larvae.
Back to the Future…
It is interesting to speculate as to how evolution will shape this emerging guest parasitism by cats of humans. If we learn anything from the study of insects, it should teach us that social guest parasites gravitate towards exploitation of the brood. House cats have eaten the fingers of babies in the past, but this isn’t a behavior that is likely to be widely tolerated. Instead, just as the staphylinid beetle A. Pubicollis induces regurgitation by its Myrmica hosts, it is possible that cats will learn to accost babies in their cribs, licking and pawing the oropharynx in a surreptitious manner to induce vomiting, then quickly consuming the regurgitated milk before a defensive response can be mounted by the human host parent.
The passing of human breast milk from the mother to the guest parasite cat via an infant intermediary could be exactly the break another emerging parasite has been waiting for. Toxoplasma Gondii is a protozoan obligate intracellular parasite with a variety of intermediate hosts, such as mice, rats, swine, cattle, and (yes) humans, but only one definitive host: the domestic house cat. T. gondii and F. sylvestris have accommodated well to each other, in that the parasite inflicts no apparent harm or damage to the cat, and the cat in turn provides ample resources in its intestine for the production of millions of parasite oocysts, which are shed in cat feces. Sporulation of the oocysts a few days or as much as a year after defecation produces the virulent form of the parasite, which can be ingested by any of the intermediate hosts. The state of diplomacy between T. gondii and the intermediate hosts, particularly mice and humans, resembles more of a smoldering insurgency. Unable to form its egg stage in these hosts, the parasite instead forms dormant cysts or bradyzoites in the host brain and muscle tissue. Famously, it alters the behaviors of the parasitized mice, causing them to lose their instinctive fear of cats and to expose themselves to easy predation. Consumption of the deranged mouse allows ingestion of the cysts and completion of the T. gondii life cycle. More controversially, latent cerebral T. gondii infection in humans has also been linked to an increase in suicidal and high-risk behaviors. But the suicide of the human fails to close the life cycle loop of the parasite since cats are generally prevented from consuming the brain or muscle of deceased persons. Meanwhile, toxoplasmosis exacts a small but continuous health toll on the human host, causing a low grade, flu-like illness in many and catastrophic birth defects when an active maternal infection is transmitted to the growing human fetus.
The next emerging zoonosis might not be an offshoot of ebola or malaria, but simply a small redirection of the human T. gondii tropism from muscle and placenta to breast tissue, where the active tachyzoite stage of the parasite would be secreted directly into human breast milk. Toxoplasmosis transmitted via breast milk has been documented in mice in controlled experiments**, but such data in humans is absent. Transfer of the partially digested milk from the infant stomach to the social guest parasitic house cat would complete the protozoal life cycle with some enormous new advantages. First, the cat would not have to kill and eat the intermediate host, but simply rob it of its stomach contents. Rather than a single transfer of protozoan back to cat, there could be hundreds of transfers over many months, with the human breast recruited as a factory for the production of T. gondii parasites. T. gondii could also use its well documented ability to influence host brain function by inducing pregnant human females to desire and to tolerate cats, especially around their nursery room. In this way, the protozoan would suddenly have full access to exploit the human as a definitive host, rather than as a biological dead end.
Humans will play more than a passive role in the evolution of this relationship. Cats currently face an exceptional negative selection pressure from their human hosts, who tend to restrain, sedate, and sterilize their guest parasites. Pet sterilization increases with household income, rising to 93% of all cats in homes with more than $35,000 in annual income. Only those individual cats who can somehow evade this ongoing mass culling will provide the genes and characteristics that typify the cat species of the future. For a cat in a wealthy American household, the best choice may be simply to get out—to flee the initial host and join the 100 million feral cats, only 3% of whom have been neutered. In this scenario, parasitism of a human household would be a transitional step in the development of cats, employed by kittens that gain an advantage over feral-raised kittens by way of the food and vaccinations they obtain from the humans. Those prompted to escape before neutering would become the dominant individuals in the feral population that breeds relatively freely. A queen cat would be a female who insinuates herself into the household just around the time the woman is pregnant, in order to establish the lucrative co-parasitism of the expected infant. By timing her own pregnancy to coincide with that of her human host, the cat could take advantage of the general chaos that surrounds the human neonatal period, increasing the odds that she would not be spayed because the overwhelmed hosts simply forgot to do it.
Cats living in the developing world and in the poorer households of wealthy countries still face a 50/50 chance of being neutered before they can reproduce. Accelerated sexual maturation and precocious mating has been observed in many species, including overexploited populations of fish, in response to this sort of inescapable early mortality.***
* Yes, they do eat cats in parts of China, but they eat everything in China, including the civet cats that first introduced the SARS virus into the world. As noted above, eating cats is probably a very bad idea in the first place, considering their close affiliation with toxoplasmosis.
** Am.J.Dis.Chld. Eichenwald, H. p307, 1948 (I was unable to read this 1948 reference without feeding money to the JAMA Paywall, which you, kind reader, will not have to do. The full PDF is available in the Reference section of my blog. After 67 years, it’s about time it became public knowledge.
*** Spayed and neutered cats do not actually die, but live on for as long as 20 years in the host living space, consuming host resources. Since these individuals are already dead in a Darwinian sense, it would be highly adaptive for the cat to develop mutations that actually kill it during or immediately after such a surgical operation. That would free the host living space for another cat, which would likely be sourced from the same breeding population as the original, now deceased neutered one. The host human would be less likely to insist on sterilizing each subsequent pet, as humans tend to grieve the loss of their guest parasites in the same manner as the actual human offspring that the cats are replacing.