The coming of the genomic age has made popular genetic explanations of traits (behavioral as well as structural) in plants, animals, and humans (see, e.g., "Genomic Sequence of Strawberry Determined"; "Silver Birch Genetics Explained"; "Genome Structure of the American Cockroach"; "Finding Nemo's Genome"; "Dolphin Genes Show Relationships between Large Brains and Energy Metabolism Similar to Humans and Elephants"; "A Complete Diploid Human Genome Reveals Some Surprises").  Because of their importance (economically, historically, and emotionally), dogs have been a common target of such studies (see, e.g., "The Genetic Basis of Coat Variation in Dogs"; "Leg Length Variation in Dogs and its Relevance to Human Mutations"; "From Toy Poodle to Rottweiler: Why Is Fido So Small (or Large)?").  But evolution is not just genomics; evolutionary studies have existed ever since Darwin, and observational biology, of animal behavior, phenotypes that reflects underlying genotypes, and elucidation of characteristics and traits that are more than their genetic determinants, have been used for decades prior to genomics for the study of the history behind development of certain traits.

This week, a multidisciplinary research team* published a paper, entitled "Evolution of facial muscle anatomy in dogs" in the Proceedings of the National Academy of Sciences USA.  The focus of the study was the differences in facial expressions between dogs and wolves that have evolved since dogs were domesticated from ancestral gray wolves 33,000 years ago.  The particular facial expression is termed "AU101"; which is "a specific facial muscle movement around the eyes ([]inner eyebrow raise) [that] seems to be particularly attractive to humans.  The movement makes the eyes appear bigger, hence more infant-like and potentially more appealing to humans.  This inner brow raise also resembles a facial movement humans produce when they are sad, potentially eliciting a nurturing response from humans (Waller et al., 2013, Paedomorphic facial expressions give dogs a selective advantage, PLoS One 8, e82686).  Juvenilia has been known in other contexts to be attractive to humans; Stephen Jay Gould, the noted Harvard evolutionary biologist, published a paper ("A Biological Homage to Mickey Mouse," in The Panda's Thumb (W. W. Norton & Company, New York, 1980) showing the gradual softening of Mickey Mouse's features to be more appealing, and a long-term study of fox domestication found retention of juvenile features as a reliable trait as the foxes became more tame around humans (see "Red Fox Genome Sheds Light on Domesticated Dogs (and Maybe Humans)").  The facial feature in question is this one:

As explained in the paper, "[t]he AU101 movement causes the eyes of the dogs to appear larger, giving the face a more paedomorphic, infant-like appearance, and also resembles a movement that humans produce when they are sad (P. Ekman, W. V. Friesen, J. C. Hager Facial Action Coding System: The Manual (Network Information Research, Salt Lake City, UT, 2002)).  The authors' (and others') hypothesis is that these adaptations elicited caregiving from humans, with resulting a selective advantage.  There is some modern evidence supporting this theory; for example, dogs that expressed this facial movement were more likely to be rehomed from shelters.  There is also some support for the notion that this type of facial expression may be important in dog-human communication.

The authors describe the results of their comparative anatomical studies between domesticated dogs (Canis familiaris) and gray wolves (Canis lupus).  These results included facial dissection and comparison of dogs and wolves and then quantified wolves' and dogs' AU101 facial movements for frequency and intensity during social interactions.  Generally, the facial musculature is the same between the two species, except for the area around the eye.  In dogs, the levator anguli oculi medialis muscle (LAOM) was "routinely" present, whereas in wolves there were fewer muscle fibers and much more connective tissue in this area.  In addition, wolves "sometimes" had a tendon where the LAOM was expected to be, and as a consequence the wolf was much less able to form expressions around the eyes than the dog.  The authors specifically noted that "wolves have less ability to raise the inner corner of their brows independent of eye squinting relaxation—the anatomical basis for the difference in expression of the AU101 movement."

These differences in musculature were correlated with the frequency of AU101 movement in studies where dogs and wolves were observed interacting with humans.  The authors concluded that these differences were caused by selective pressure imposed during domestication.

The authors were express regarding the significance of their observations:

Dogs were shaped during the course of domestication both in their behavior and in their anatomical features.  Here we show that domestication transformed the facial muscle anatomy of dogs specifically for facial communication with humans.  A muscle responsible for raising the inner eyebrow intensely is uniformly present in dogs but not in wolves.  Behavioral data show that dogs also produce the eyebrow movement significantly more often and with higher intensity than wolves do, with highest-intensity movements produced exclusively by dogs. Interestingly, this movement increases paedomorphism and resembles an expression humans produce when sad, so its production in dogs may trigger a nurturing response.  We hypothesize that dogs' expressive eyebrows are the result of selection based on humans' preferences.

And they concluded that:

Overall, the data suggest that selection—perhaps mainly unconscious—during social interactions can create selection pressures on the facial muscle anatomy in dogs strong enough for additional muscles to evolve.  This opens up interesting questions for future research, such as questions on other domestic species like cats and domestic horses and also breed differences in dogs as well as questions on the kind of selection pressure necessary for this to emerge.  One highly relevant question in this regard would be whether selection for tameness alone might create the same scenario.  Here the domesticated silver foxes . . . would be relevant and interesting model taxa.

Observational biology was once the hallmark of the discipline, when it was termed natural history.  Theodeous Dobzhansky once famously explained to a graduate student perplexed by the complexity of polytene chromosomes in Drosophila melanogaster and having a difficulty in recognizing characteristic patterns that he did so the same way he recognized the different faces of the members of his laboratory.  While the power of modern genetic analysis has provided deep explanations of everything to the genetic basis for (some) disease to the development of related populations of the human family (see David Reich, Who We Are and How We Got Here: Ancient DNA and the New Science of the Human Past), we would do well to remember that, as Darwin said:

There is grandeur in this view of life, with its several powers, having been originally breathed by the Creator into a few forms or into one; and that, whilst this planet has gone cycling on according to the fixed law of gravity, from so simple a beginning endless forms most beautiful and most wonderful have been and are being evolved.

* Authors from the Centre for Comparative and Evolutionary Psychology, Department of Psychology, University of Portsmouth, United Kingdom; the Department of Anatomy, Howard University College of Medicine; the Department of Biological Sciences, North Carolina State University; and the Department of Physical Therapy, Duquesne University.