Yesterday I got a call from the outside

world but I said no in thunder.

I was a dog on a short chain

and now there’s no chain.–Jim Harrison (from “Barking”) This won’t be big news to you, but some people have dogs, in their houses. Dogs are domesticated wolves. They are wolves capable of spending long days inside on designer pillows, wolves often dressed in ridiculous outfits, wolves in civilization’s trampy clothing. They are no longer wild, yet capable, as anyone knows, of wildness. If I walk around my neighborhood, I see these wolves dragging their people to the park, around the block, or further. These wolves affect their people. They take them places. They make them happy. But, new studies suggest, they also do more, they connect them, invisibly, literally, to a richer life.

I grew up with dogs, multiple dogs, dogs named after the things they did (Puddles), pieces of meat (T-bone), elderly neighbors (Betsy), money (Penny) and general demeanor (Buster). I grew up with dogs in the country. These were not the sort of dogs whose still-warm poop is scooped up in plastic bags. These dogs shat in the woods. These dogs sometimes disappeared for a few days only to return, dirty, stinking and a little bit skinnier or—and this happened just once—quite a bit fatter.

One Thanksgiving, just as we were getting ready to sit down to eat, my dog Penny, a stubby half-beagle, came stumbling out of the woods looking decidedly fat and sick. As she stumbled, we saw that she was dragging a turkey. The turkey was still in its wrapper, except for the hole through which Penny had inserted her head long enough to engorge on about 1/3 of the quite large, still-frozen, bird. In rural Michigan, where I grew up, it was common to leave your turkey, too large for your refrigerator, in your garage to defrost. Penny, it appears, struck doggy gold. To the neighbor of mine who has a Thanksgiving story that begins, “It was the year of the disappearing turkey,” I apologize.

Image 1. An ancient Greek drinking vessel in the shape of a dog’s head. We have been drinking of whatever dogs bring us for a long time. This particular vessel was made by Brygos in 5th century BC. It now lives in the Jérôme Carcopino Museum, Department of Archaeology.

I tell you about Penny to establish what we all know, that dogs can bring a variety of things to us. Sometimes their gifts are literal—a mangled turkey—other times they are more figurative. Personally, the smell of wet dogs (which almost certainly comes from their microbes) reminds me of running through the forest, chasing my dogs as they chased some wildness tree to tree into a deeper wood. Collectively, dogs remind us all of what it means to be more wild — an effect that, it turns out, is not just psychological. Dogs link us to wild landscapes in at least ten ways, each of which is of consequence for the simple reason that there are now so damned many dogs, perhaps half a billion, perhaps more (WHO-WSPA 1990), sniffing through civilization’s rank corridors and then beyond.

1 – In our backyards and forests, dogs affect which other animals are present. They chase out many animals we would rather have around. Dogs kill wild sheep, deer, gazelles, rabbits, iguanas, birds and more. The effects of roaming dogs on small mammals can be tremendous and negative. In some places, feral dogs are now the most abundant predators1. They lunge out from their pens, chains and yards and diminish what once was.

2 – In houses, dogs calm us psychologically, providing companionship and reducing stress, unless we are an intruder or someone who meets a dog behaving badly in which case, well, some dogs, of course, can bite or even kill us. One of the original reasons for the domestication of dogs was undoubtedly as protection, whether from other animals or from other humans, but our protectors can go wrong. Dogs attack more people than any other predator. 2 When they do, they recall the dangerous possibilities of their (and our) bodies and teeth.

3 – The same body that can kill, can also warm. In ancient cities, dogs may have saved lives by preventing their owners from freezing to death. Those hairless, Peruvian dogs with their yellow mohawks are reported to have protected the cold body of many an Incan official3. The native peoples of Australia also seem to have appreciated dog heat, “on cold nights they slept with their dingoes to keep warm (though the English are said to have preferred to warm themselves on pigs).” Dogs still warm us with that same, canine heat.

4 – In our modern cities, dogs provide feces where none is asked for. In some cities, for example certain well-known French cities (OK, Paris), this feces piles up as if in protest against domestication. In other cities, it is carefully removed. Most cities seem to be somewhere in between. As a result, enough feces is on the ground in these cities that the air above cities is thick with the microbes associated with dog shit4. The ground, in other cities, particularly those with many feral dogs, is dense with dog-associated parasitic worms, worms that can infect and affect both humans (no fewer than sixty parasites found in dogs can infect humans) and, in some cases, other wildlife5. Canine distemper in wild lions and Lake Baikal seals (Phoca sibirica) came from domestic dogs, as, it seems, did the lice now found on Alaskan wolves.

But the effects I’ve been thinking about lately have to do with bacteria inside houses and allergies. In one study in Detroit, the health of pregnant women (and their newborns) with dogs in their homes was compared to that of those who did without. Researchers examined the effect of having a dog on one indicator of an individual’s tendency to develop allergies: the level of IgE antibodies in the mother’s umbilical cord blood. Which brings us to…

5 – What these researchers found: pregnant mothers who lived in houses with dogs tended to have lower levels of IgE antibodies in their cord blood—and such lower levels have been found to be protective when it comes to childhood allergies6. This study like any study, had limits. The number of women considered was relatively small. In addition, the study was not experimental. The dogs were not given randomly to women irrespective of their interest in having a dog. But who are we kidding? There ain’t a researcher in the world dumb enough to try to force a pregnant woman who doesn’t want a dog to take care for one, at least none who have survived.

6 – The researchers studying pregnant mothers posited that the effect of the dogs is due to the effect of dogs on the microbes in the house and on and even in the body. Initially, this argument was pure speculation, but in 2010 another group of researchers considered the microbes in six houses with dogs and five without. Their goal was specific, figuring out which microbes were present. They seemed to find a difference, though they were appropriately cautious in interpreting it, stating that the diversity of bacteria in the dog houses seemed higher than that in the no-dog houses7 . Interestingly, fungal diversity seemed lower in dog houses (though again, the sample size was very small).

7 – A more recent study has shown that children with pets in general (primarily dogs) are at a reduced risk of childhood wheezing (which is associated with allergy and asthma). The study also found that one common bacteria species, generally thought of as a beneficial gut microbe, Bifodobacterium longum, was more abundant in those children exposed to pets than those who were not exposed to pets and suffered from wheezing8.

I am not an expert on dogs or their effects on humans, so the above list is probably partial. Dogs have lived with us for more than 10,000 years and they do so today in great abundance, about one dog per every three adult humans on Earth and so they connect us to the rest of life in many different ways in many different places. Forgive my omissions. Other than occasionally bemoaning the number of books about people and how much they love their dogs, as a writer I don’t deal with dogs much. I wrote once about what dogs are really sniffing when they go for your crotch, but that was really an article about crotches as much as it was one about dogs. There seem to be enough dog writers. Neither do I tend to do research on dogs. I once had an undergraduate student, Meredith Spence, do a project on which of the parasites of North American carnivores sometimes turn up in dogs (most of them), but then Meredith moved on to better things and I left the dogs alone, which I planned to continue to do, but then, like my dog Penny dragging the turkey, the dogs came back.

Along with Noah Fierer at the University of Colorado (who I have finally met in person after nearly three years of collaboration. Thankfully, we get along, as do our kids), Jon Leff, Jessica Henley, Holly Menninger, and a team of more than a thousand citizen participants, we have been studying the ecology of microbes in homes. The goal of this project, called the Wild Life of Our Homes and funded by the Sloan Foundation, is to understand what governs which microbe species—be they fungus, bacteria, archaea or other—live in a given home. It compliments other work funded by the Sloan Foundation, for example a project designed by Jack Gilbert and his swab-happy crew to understand, when people move into new homes, what proportion of the microbes are given to the home by the people and vise versa. And work by Jessica Green’s team at the University of Oregon to understand the effect of opening windows on the microbes inside houses.

Image 2. Noah’s (recently deceased) dog Gunther whose bacteria live on inside Noah’s house.

In our project, we work with citizens who sample their own houses. Our participant-collaborators send in swabs of their houses (and often little prizes for us, drawings and the like, for which we are grateful). In two houses in each of 50 states our participants even install data loggers to monitor the climate of their homes (much as if we were tracking storms in the Amazon).

Our very first step in this project was to understand how much variation there is among habitats within a given home and so in a set of eighty homes in Raleigh and Durham, North Carolina, we had participants sample nine habitats in their homes. Once we extracted, amplified and sequenced DNA from the first forty of these homes (which takes us some time and thus the citizens get to experience both the joys and the mind-numbing monotony of science), we saw very clearly that different habitats in the home are host to very different microbes—in essence we found three main habitat types, at least from the places we sampled, a habitat associated with food, one associated with human bodies and one associated with the outdoors. But no two samples of any habitat were exactly the same in any two homes. Why? What makes your counter so different from mine? That is what we really wanted to get at. This is where the dogs came in, barking, yapping, slobbering and shedding.

Image 3. On the left are the 9 locations sampled by our citizen scientists (Image Credit: Neil Mccoy & Hayley Stansell). On the right is a plot representing the microbial communities we detected on the 9 surfaces in the 40 homes. Each dot represents the microbial community detected on one surface in one home (We graphed the results of 40 homes, so there are 360 dots on this plot). The dots are color-coded by surface-type. The axes of the graph don’t mean so much – Rather, focus on the extent to which different colored dots overlap and cluster. Those colors that strongly overlap in space have very similar microbial communities (e.g. the places we touch: toilet seat, pillow case, and door handle); those colors that cluster far apart from each other have very different microbial communities (i.e. toilet seat/pillow case vs. exterior door trim).

In comparing homes, we investigated a number of factors that might be important in terms of explaining differences in the bacteria among homes (And here by “we” I mean Jon Leff). Some, such as the presence of carpet in a house or the frequency of antimicrobial use, showed interesting patterns, but none explained much variation. Then we began to look at pets. About a third of the houses in our study had dogs; very few of the houses exclusively had cats so we focused on dogs (Cat lovers, we promise to return to the cats when we consider all the houses). We tested whether the presence or absence of a dog explained some of the variation among the houses we sampled. Now here I should say that the expectation was that they would explain little. The houses we considered differed in many features—number of occupants, presence of children, recent use of pesticides, presence of carpet—such that it seemed unlikely any one variable would explain much of the variation. Then we looked at dogs. The presence or absence of a dog in a house explained nearly half of the variation in the bacterial composition on pillows and TV screens in the houses we studied, NEARLY HALF!

I was shocked. There was more here, more differences, more to study, but before we got to that, we needed to figure out what was going on with the dogs. It appears that the bacteria the dogs are bringing in are not random. On the pillows in homes, dogs are bringing in bacteria associated with their mouths (such as spirochetes and species of Pasteurellaceae), their skin and fur and soil. On TVs, the bacteria tended to be those associated with soil, dog skin and, well, we aren’t quite sure. These were not fecal bacteria. The fecal microbes we found in homes tended to be those associated with humans, not dogs.

The next question we’ll tackle is how consistent this effect is. There are already hints. At the recent American Society of Microbiology meeting, Jack Gilbert and his crew indicated that they too had found that, in their seven houses in Chicago, the biggest differences among houses is due, again, to the presence of dogs.

8 – Recently, another study found that humans tend to pick up, on their skin, some microbes from their dogs; dog owners tend to share more microbes with their dogs than with random dogs (evidence that, at least microbially, dog owners really do become more similar to their dogs over time). The links between our bodies and our houses and our dogs’ bodies seem to be direct and intimate.

How do we pull all of this together? If I was going to write a dog book, this is where I would say that my dog Penny made me who I am and that this was in part due to the microbes she shed upon me. Oh Penny, I couldn’t have done it without you!

9–But this is not a book about dogs, it is a research program about houses into which dogs have trotted out of the dark without being beckoned and so instead I’ll suggest a hypothesis for just what it is that our dogs are doing in our homes. Once, our dogs were our mutualists. We benefited them and they us; today our relationship is more complex. But I hypothesize that our dogs still affect our fitness. They do so when they bring bacteria to us. They bring it in their mouths, on their skin and in their fur, but also from the dirt around our homes (this much is not speculative, it now seems well-supported). I hypothesize that some people, particularly a subset of individuals living in very urban environments, environments in which their fingers rarely sink deeply into the mud, are so deeply removed from the diversity of wild species that their immune systems fail to develop normally (this also seems rather well supported). Finally (this is the bit in which I lean out into the darkness and wave my hands), I hypothesize that in these latter settings, settings like those found in many suburbs and most cities, dogs reconnect us to a diversity of species, species they drag into our houses, species that in the absence of more robust connections to microbial diversity may be sufficient to bring sense to our immune system. The connection dogs offer is not perfect (we might achieve a similar effect, other studies suggest, by living on a farm, or even planting native species in our backyards), but it can sometimes be enough in a world in which we have so few direct connections to life’s richness. In other words, while our dogs sometimes bring us frozen turkeys, they may,other days, bring us health. This is where the dogs are pointing as they run down the path barking, back to the biodiversity from whence we, and even the dead turkey, all came. It is an effect balanced by the other effects of dogs and yet one we experience (or fail to experience) all the same.

10–Lest you wonder about your cat or about the effect of one kind of dog over another or the effect of a weasel or a goat or chicken, we are on it. We are in the process of processing samples from the houses of 1400 of our participants across North America, houses that span a diversity in terms of their domesticated occupants, houses that, I suspect, will soon have me, once again, writing about dogs.This is the tenth way dogs affect you, the way we don’t yet know, but will soon. Fourteen hundred yellow envelopes, each filled will four samples of a house, are, as we speak, being ready to be shipped from my lab to Noah’s where, by looking at the tiny life on ordinary swabs, we will see.



Footnotes

1-BioScience 61: 125–132. ISSN 0006-3568, electronic ISSN 1525-3244.

2-My postman, personal communication.

3-http://onlinelibrary.wiley.com/doi/10.1111/j.1439-0388.1984.tb00043.x/abstract

4-Applied and Environmental Microbiology, Sept. 2011, p. 6350–6356 Vol. 77, No. 18. doi:10.1128/AEM.05498-11

5- Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 14, No. 1, January 2008

6- Bergmann RL, Edenharter G, Bergmann KE, Guggenmoos-Holzmann I, Forster J, Bauer CP, et al. Predictability of early atopy by cord blood-IgE and parental history. Clin Exp Allergy 1997;27:752-60. Aichbhaumik N, Zoratti EM, Strickler R, Wegienka G, Ownby DR, Havstad S, et al. Prenatal exposure to household pets influences fetal immunoglobulin E production. Clin Exp Allergy 2008;38:1787-94.

7- K. E. Fujimura, C. C. Johnson, D. R. Ownby et al., “Man’s best friend? the effect of pet ownership on house dust microbial communities,” Journal of Allergy and Clinical Immunology, vol. 126, no. 2, pp. 410.e3–412.e3, 2010.

8- http://dx.doi.org/10.1155/2013/827934

9- Song et al. eLife 2013;2:e00458. DOI: 10.7554/eLife.00458