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'Puppy-dog eyes' produced by evolution

September, 2019

If you are a dog owner, you likely think of your dog as a true friend — a creature you can relate to and who relates to you. This connection doesn't need words. Perhaps your dog looks up at you and makes those big puppy-dog eyes, and you know his meaning: time for a treat! New research suggests this phenomenon is neither an accident nor your imagination. Domestic dogs' ability to communicate with us via facial expression is instead the result of tens of thousands of years of dogs' evolution alongside humans.

Where's the evolution?

It's common knowledge that the distinct traits of the hundreds of different domestic dog breeds are the result of human manipulation of evolution. For the last 200 years, humans have opted to breed animals with traits that better served our purposes, generation after generation. For example, favoring dogs that were better at pulling sleds through Arctic snow led to the evolution of the husky; while favoring dogs better at retrieving wild game from the water and pulling fishing nets led to the Chesapeake Bay Retriever. Still other dog breeds were selected for more whimsical, less practical purposes. The Yorkshire Terrier, for example, resulted from breeders' preference for long, silky fur. These are classic examples of artificial selection in action.

The Siberian Husky, Yorkshire Terrier, and the Chesapeake Bay Retriever

It wasn't just outward aspects of dogs' anatomy that we shaped through artificial selection. In the last 15,000 years, while living alongside humans, domestic dogs have diverged from their closest relatives, grey wolves, in many ways. Unsurprisingly, our ancestors seem to have selected for animals that better fit into human societies, resulting in dogs that were less wary of humans and less aggressive, with smaller teeth and shorter snouts.

Now new research suggests that we were also (likely unintentionally) favoring dogs that reminded us of ourselves and human children — in particular, dogs able to pull their inner eyebrows up to make a face that looks a bit "sad" to us. This eyebrow raise is performed by a little muscle with a big name (the levator anguli oculi medialis, LAOM for short). Researchers studied the facial anatomy of domestic dogs and grey wolves, and found that while most muscles in the face were similar in the two groups, the LAOM was much larger in domestic dogs. This larger size translates into more movement, the scientists also found. Dogs raise their inner eyebrows more often than wolves do, and dogs raise their eyebrows higher than wolves do.

These observations alone would be a suggestive "just-so" story, but probably not enough to convince an evolutionary biologist that puppy-dog eyes evolved through human artificial selection. However, other lines of evidence also support this idea. For example, researchers studied domestic dogs in a shelter and found that those that made puppy dog eyes more often were adopted sooner than others. Thus, among shelter dogs, making big puppy dog eyes provides a survival advantage by appealing to human caretakers. If puppy dog eyes boost survival today, it seems likely that, during domestic dog evolution, the trait also conferred a survival and reproductive advantage — and hence, higher evolutionary fitness.

Comparative studies of wolves and dogs further suggest that puppy dog eyes represent just one of a suite of traits that evolved during domestication and allowed dogs to better communicate with and appeal to humans. Dogs understand human communication cues like pointing better than wolves (or even chimpanzees, our closest living relatives) do. Dogs use human eye contact as a way to ask for help, while wolves do not. And finally, sustained eye contact between dogs and humans (i.e., "mutual gaze") leads to a positive hormonal response (an oxytocin feedback loop, similar to the one that occurs when a mother and her infant gaze at one another) from each species, but does not occur when wolves and humans look at one another.

Based on all this, scientists think it is plausible that some traits of ancestral domestic dogs happened to trigger human caregiving responses, which originally evolved in the context of parent/child interactions. Dogs that expressed such traits benefited from more human care and perhaps favoritism, and so were more likely to survive and reproduce than dogs that did not. Over time, through the accumulation of small variations in these triggers (extending eye contact for a bit longer, having a larger LAOM and producing slightly more heartbreaking eyes, etc.), the connection between domestic dogs and their humans evolved to be even closer.

This hypothesis suggests that evolution, in some ways, "hijacked" the human caregiving response — i.e., a trait that initially evolved in the context of benefitting human offspring wound up also benefitting another species. However, this does not mean that dogs themselves are intentionally manipulating us or that they evolved any traits "in order" to get closer to humans. Evolution does not occur because of need or effort. It simply retains traits that boost survival or reproduction — in this case, a trait that is easily conflated with intentional manipulation or effort. And of course, humans likely also benefitted from their association with dogs, gaining additional protection and a domestic animal that could be put to use in many ways — as a hunting partner or sled puller, for example. So the next time a puppy looks up at you with those big eyes and tugs on your heartstrings, go ahead with the "awwwwww" and the ear rubbing; your ancient human ancestors probably did the same.

Read more about it

Primary literature:

  • Kaminski, J., Waller, B. M., Diogo, R., Hartstone-Rose, A., and Burrows, A. M. (2019). Evolution of facial muscle anatomy in dogs. Proceedings of the National Academy of Sciences USA. 116: 14677-14681.read it
  • Ostrander, E., Wang, G., Larson, G., vonHoldt, B. M., Davis, B. W., Jagannathan, V., Hitte, C. ... Dog10K Consortium. (2019). Dog10K: an international sequencing effort to advance studies of canine domestication, phenotypes and health. National Science Review. Nwz049. https://doi.org/10.1093/nsr/nwz049. read it
News articles:

Understanding Evolution resources:

Discussion and extension questions

  1. Review the process of natural selection here. Explain the differences and similarities between the processes of natural selection and artificial selection.
  2. In a series of steps, explain how dogs might have evolved a larger LAOM during the process of domestication. Be sure that your explanation includes the concepts of variation, inheritance, and selection.
  3. Describe two lines of evidence that support the hypothesis that ancient dogs experienced artificial selection affecting their facial expressions.
  4. Imagine that a friend skims an article on the new dog domestication research and then makes a series of claims. How would you respond to each to explain things more accurately? (Reviewing some misconceptions about natural selection and adaptation may help.)
    1. "See? That's why I've always preferred cats. Dogs evolved those silly, sad eyes in order to mooch off of humans!"
    2. "If cats wanted to, they could evolve a lot quicker than dogs did. They are much smarter and figure things out faster."
    3. "Just goes to show why exercise is so important. Even tiny muscles get a lot bigger over time if you use them a lot!"
  5. Advanced: In places like the United States, where most domestic dogs live with people at their homes, are dogs currently evolving through unintentional artificial selection by humans? Explain your reasoning, and if your answer is yes, explain which traits might be evolving. (Note that this question excludes intentional artificial selection involved in selecting breeding stock for show or work dogs.)
  6. Advanced: In places where most domestic dogs roam more freely, associated with human society but not "owned" by a human, are dogs currently evolving through unintentional artificial selection by humans? Explain your reasoning, and if your answer is yes, explain which traits might be evolving.
Related lessons and teaching resources

  • Teach about natural selection: In this classroom activity for grades 9-16, students simulate breeding bunnies to show the impact that genetics can have on the evolution of a population of organisms.
  • Teach about the process of artificial selection: In this classroom activity for grades 6-16, students learn how artificial selection can be used to develop new dog breeds with characteristics that make the dogs capable of performing a desirable task.
  • Teach about studying evolution in the wild using artificial selection: This research profile for grades 9-16 follows scientist David O. Conover as he investigates the impact of our fishing practices on fish evolution and discovers what happened to the big ones that got away.

References

  • Kaminski, J., Waller, B. M., Diogo, R., Hartstone-Rose, A., and Burrows, A. M. (2019). Evolution of facial muscle anatomy in dogs. Proceedings of the National Academy of Sciences USA. 116: 14677-14681.
  • Ostrander, E., Wang, G., Larson, G., vonHoldt, B. M., Davis, B. W., Jagannathan, V., Hitte, C. ... Dog10K Consortium. (2019). Dog10K: an international sequencing effort to advance studies of canine domestication, phenotypes and health. National Science Review. Nwz049. https://doi.org/10.1093/nsr/nwz049.  
  • Parker, H. G., Kim, L. V., Sutter, N. B., Carlson, S., Lorentzen, T. D., Malek, T. B., Johnson, G. S., ... Kruglyak, L. (2004). Genetic structure of the purebred domestic dog. Science. 304: 1160-1164.