Absolute Brain Size Predicts Dog Breed Differences in Executive Function

Daniel J. Horschler1,*, Brian Hare2,3, Josep Call4,5, Juliane Kaminski6, Ádám Miklósi7,8, & Evan L. MacLean1

Supplementary Material

1School of Anthropology, University of Arizona, Tucson, AZ, 85719, United States 2Department of Evolutionary Anthropology, Duke University, Durham, NC, 27708, United States 3Center for Cognitive Neuroscience, Duke University, Durham, NC, 27708, United States 4Department of Developmental and Comparative Psychology, Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany 5School of Psychology and Neuroscience, University of St Andrews, St Andrews, United Kingdom 6Department of Psychology, University of Portsmouth, Portsmouth, United Kingdom 7Department of Ethology, Eötvös Loránd University, Budapest, Hungary 8MTA-ELTE Comparative Ethology Research Group, Budapest, Hungary *Correspondence - Email: [email protected]; Phone: 520-621-2646 Method Details

Cognitive Data. Cognitive data were compiled from the Dognition.com database.

Dognition.com is a citizen science website that provides dog owners with instructions for completing cognitive experiments with pet dogs in their homes. Participants receive written and video instructions for the behavioral protocols, and electronically submit data on their dog’s responses as activities are completed. We included data from ten cognitive tasks in our analyses:

Yawning, Eye Contact, Arm Pointing, Foot Pointing, Cunning, Memory vs. Pointing, Memory vs. Smell, Delayed Memory, Inferential Reasoning, and Physical Reasoning. For detailed protocols of each task, see Task Details.

We analyzed all subjects from a dataset originally including 18,610 dogs, with the majority of these dogs having completed multiple tasks. To ensure that our sample included only adult dogs, we removed all data from dogs who were 1 year or younger at the time of testing (n =

2,307). Because our analyses focused on breed-average performance, we eliminated data from dogs that were identified as mixed breeds, or for whom the breed identity was not known (n =

5,311; both measures determined by owner report). We also eliminated data from a small subset of with reported body weights intermediate to miniature and standard morphs (n = 22, see Morphological Data). Lastly, to ensure representative samples across breeds we removed data from breeds represented by less than 20 individuals (on a task-wise basis), as well as for breeds which lacked body weight or genetic data (n = 3,573 individuals) from the primary sources these data were compiled from (see below). The final dataset we analyzed included

7,397 dogs. Demographic data for each breed included in our analyses is shown in

Supplementary Table 1. Data Collection Process. All text in this section and in the following Task Details section was directly adapted from Stewart et al. (2015). All participants received instructions recommending cognitive tasks be conducted at home in a familiar room reasonably free of distractions. Participants were encouraged to take breaks whenever the dog lost motivation, and were repeatedly reminded not to intentionally influence their dog’s choices, although experimental evidence suggests that the effect of unconscious cuing on dogs during cognitive experiments may not be as ubiquitous as has often been suggested (Hauser, Comins, Pytka,

Cahill, & Velez-Calderon, 2011; Pongrácz, Miklósi, Bálint, & Hegedüs, 2013; Schmidjell,

Range, Huber, & Virányi, 2012). Regardless, instructions were worded to frequently remind participants that there “are no correct answers” and to let their dog choose freely.

For each task, participants watched a how-to video that detailed the experimental setup, procedural protocol, and the set of possible responses from their dog that they would need to live code. Written instructions and a Frequently Asked Questions (FAQ) section were also provided, and a link to the FAQ was available at all times in case questions arose during testing.

Participants were not able to advance through tasks or trials out of order, to help ensure that participants correctly followed all steps, and repeated each trial the correct number of times.

Once all of the steps were complete for each trial, participants were asked to code their dog’s behavior. The majority of decisions involved either stopping a timer or indicating which of two locations the dog approached first.

Participants were instructed to work with a partner unless their dog was able to sit and stay on their own. Video and written instructions emphasized the importance of staring directly ahead after releasing the dog, and of releasing the dog without nudging, pushing, or leading the dog in one direction or the other. In the instructional video, the dog was positioned directly across from the experimenter, approximately 1.8m away. Three post-it notes were placed on a line perpendicular to the dog and the experimenter. The center post-it was placed 0.6m directly in front of the experimenter, while the other two were placed 0.9m on either side of the center post-it. Once participants completed this set up, they advanced to step-by-step instructions for each trial.

Task Details. The vast majority of dogs were tested using the following task order:

Yawning, Eye Contact, Arm Pointing, Foot Pointing, Cunning, Memory vs. Pointing, Memory vs. Smell, Delayed Memory, Inferential Reasoning, and Physical Reasoning. Non-differential rewarding (in which any choice was rewarded) was used in Arm Pointing, Foot Pointing, and

Cunning, while differential rewarding was used in Memory vs. Pointing, Memory vs. Smell,

Delayed Memory, Inferential Reasoning, and Physical Reasoning.

Task Details: Yawning. The Yawning task procedure was based on Joly-Mascheroni et al.

(2008). Participants watched a video of instructions that included examples of dogs yawning.

Participants were instructed to sit on the floor with the dog, but not to touch or interact with the dog at any point during the yawning conditions. In the control condition, the participant was prompted to say the word “yellow” every 5 seconds for 30 seconds. In the experimental condition, the participant was instructed to yawn clearly and audibly every 5 seconds for 30 seconds. Once this 30-second period ended, a 2-minute timer started. During the 30-second manipulation and the 2 minutes that followed, the participants were instructed to observe if the dog yawned. They were prompted to code whether the dog yawned after each trial (they were not asked for a frequency). There was only one trial of each condition, and all subjects received the control condition first. Task Details: Eye Contact. Procedurally, the Eye Contact task was based on Nagasawa et al.

(2009). Participants first conducted a warm-up condition, in which the participant was instructed to stand facing their dog with the dog standing or sitting ~1.8 meters away. The participant was then prompted to call the dog’s name, show the dog a small treat, and place that treat directly beneath their eye and to start the 10-second timer. Once time elapsed, the participant was prompted to give the dog the treat. No coding was required and the warm-up was repeated three times. The experimental condition was the same as the warm-up except that the participant was instructed to stop the timer once the dog broke eye contact for more than two seconds. If the dog never broke eye contact, the trial ended after 90 seconds. Three trials of this condition were conducted.

Task Details: Arm Pointing and Foot Pointing. The Arm Pointing task was based on Gácsi et al. (2009) while the Foot Pointing task was based on Lakatos et al. (2009). In the pointing warm- up, the dog was introduced to the two potential locations to find a treat. The participant was instructed to stand ~1.8m away from the dog, call the dog’s name, show the dog a treat, and place the treat down on the ground at arm’s length to either the left or right (~1.2m apart). The instructions indicated which side to place the treat on in each trial. The treat location was counterbalanced across trials and participants never placed a treat on the same side on two consecutive trials. Once the participant had placed the treat, they were instructed to release the dog while giving a release command. After each trial, the participant was asked to record if the dog retrieved the treat. There were six trials in this warm-up.

The Arm Pointing and Foot Pointing conditions were identical to the warm-up except that two identical food treats were placed at arm’s length on either side. Participants were instructed which location they were to gesture toward and to allow the dog to retrieve both treats while recording which location the dog approached first. A first approach was illustrated in the video and was defined as crossing the plane created by the post-it notes on the left or right. In the Arm

Pointing condition, participants were to point by extending their arm, hand, and index finger toward one location while standing equidistant between the two locations. In the Foot Pointing condition, participants were instructed to take one step toward one location while extending their leg and food in the direction of the other location. In both experimental conditions, gaze and gesture was to be directed at the location being indicated until the dog made their choice. Six trials were conducted in each condition.

Task Details: Cunning. The Cunning (Other’s Visual Cues) task was procedurally based on

Call et al. (2003). In the baseline watching condition, the dog was positioned ~1.8m from the participant. The participant was then instructed to say the dog’s name and “No” or “Leave it” twice, clearly and loudly, while placing a treat in front of them on the ground. Once the participant stood back up, they activated the countdown timer, which they only stopped when the dog approached and ate the forbidden food. The timer automatically stopped after 90 seconds if the dog never approached. The two experimental conditions were identical to the baseline condition except that the participant did not watch the treat. In the back turned condition, the participant immediately turned their back to the dog, while in the eyes covered condition, the participant covered their eyes with their hands. If a partner was helping, they were also instructed to turn their back. Participants were instructed to look over their shoulder every few seconds or to peer through their fingers subtly to detect when the dog approached. Two trials of the back turned and eyes covered condition were conducted. One watching trial was conducted before and after the four experimental conditions. The two back turned conditions always preceded the eyes covered trials. Task Details: Memory vs. Pointing, Memory vs. Smell, and Delayed Memory. Dogs were first introduced to finding food hidden underneath cups. The participant started by standing

~1.8m away from the dog, and placing one opaque cup upside down on the left or right at arm’s length (~1.2m apart). In the first condition of the warm-up task, the participant was instructed to call the dog’s name and show the dog a treat. The participant then placed this treat underneath the cup as their dog watched. The second warm-up condition was the same as the one-cup warm- up except the participant placed a cup at arm’s length on both the left and right simultaneously.

Then they placed a treat under one of the two cups as their dog watched. The treat location was counterbalanced across trials and participants never placed a treat on the same side on two consecutive trials. Once the treat had been placed under the cup, the participant gave a release command. A first approach was illustrated in the video and was defined as crossing between the plane created by the center-left or center-right post-it notes. If the dog chose the side with the treat, the dog was allowed to eat the treat. If the dog chose the side without the treat, the participant was instructed to show the dog where the treat was located, but to prevent the dog from eating the treat. After each trial the participant was prompted to record if the dog retrieved the treat. Four trials of each warm-up condition were administered for a total of eight warm-up trials.

The Memory vs. Smell procedure was based on a similar comparison in Szetei et al.

(2003). This task was identical to the two-cup warm-up, except that while the dog’s view was occluded, the treat was switched to the opposite cup in which it was initially hidden (suggestions for blocking the dog’s view included (1) covering the dog’s eyes with the partner’s hands, (2) turning the dog around while distracting it, or (3) kneeling in front of the dog while holding its head). Four trials were conducted. The Memory vs. Pointing procedure was also was based on a similar condition in Szetei et al. (2003). Memory vs. Pointing was identical to the two-cup warm-up except that once the food was hidden, the participant extended their arm, hand, and index finger toward the empty cup. Six trials of this condition were conducted.

Finally, the Delayed Memory procedure was based on Fiset et al. (2003) and MacLean et al. (unpublished data). The Delayed Memory task was the same as the two-cup warm-up except that after the food was placed, participants waited increasingly longer delays before releasing their dog to search for the hidden food. In the first trial the countdown timer ran for 60 seconds, increasing by 30 seconds per trial for three more trials. The delay for the last trial lasted for 150 seconds.

Task Details: Inferential and Physical Reasoning. The Inferential Reasoning task was based on the procedure of Erdohegyi et al. (2007). In a warm-up condition, the participant was instructed to stand ~1.8m away from the dog, and to place two cups at arm’s length to the left and right (~1.2m apart). Both cups were placed on their side with the inside of the cup facing the dog. The participant was then instructed to call the dog’s name and show the dog a treat. The participant then blocked the dog’s view of the treat in their hand with an opaque occluder. They next baited one cup while sham baiting the other. Regardless of where the treat was hidden, the participant was instructed to always move from the right cup to the left cup. The treat location was counterbalanced across trials and participants never placed a treat on the same side on two consecutive trials.

Once the participant had baited or sham-baited both the right and left cup, they placed the barrier behind them and left the cups laying flat with open sides facing the dog (so that the dog could easily see the treat in one of the cups). To help the dog see the treat clearly, the participant lifted both cups simultaneously, bringing them together at the dog’s approximate eye level. They then placed them upside down to hide the food’s location. Dogs simply had to remember where they saw the food hidden when released. After each trial, the participant was asked to record if the dog retrieved the treat. Six trials of this warm-up were conducted.

In the Inferential Reasoning task, the procedure was the same as the warm-up except that after baiting the cups, they were flipped upside down without showing the dog where the food was hidden. Then the participant showed the dog which cup was empty by lifting the empty cup and bringing it to the dog’s approximate eye level. After placing the empty cup back down, the dog was released to search. Four trials of this experimental condition were conducted.

In the Physical Reasoning task warm-up, the participant folded two pieces of standard

U.S. (8.5” x 11”) paper width-wise so that when placed on the ground, they remained flat. One piece of paper was then placed at arm’s length on the left or right. The participant was then instructed to call the dog’s name and show the dog a treat. They next occluded the baiting of the hiding location by holding an opaque barrier in front of the hand with food. The participant then wedged the treat in the crease of the paper, propping one side of the paper up. Once the participant had hidden the treat, they placed the barrier behind them and the dog was released to search. If the dog approached close enough to touch the paper, the participant could either let the dog open the paper or fold the paper down to help the dog access the food. If the dog did not approach the paper after 90 seconds, the participant would show the location of the treat to the dog and allow him/her to eat it. After each trial, the participant was asked to record if the dog retrieved the treat. There were four trials in this condition.

In the Physical Reasoning experimental condition, based on Bräuer et al. (2006), the procedure was the same as the warm-up except that the participant placed a folded piece of paper on the left and right at arm’s length. They then occluded the baiting and sham-baiting as they propped one of the pieces of paper up using the treat. Counterbalancing was automated so that the first side baited alternated equally between left and right across dogs and within the test session of any one dog. After each trial, the participant was instructed to record if the dog retrieved the treat. There were four trials in this condition.

Morphological Data. As a measure of breed-typical body mass, we used breed-mean body weights from the Canine Behavioral Assessment and Research Questionnaire (C-BARQ).

The C-BARQ is a 100-item survey completed by dog owners and used to quantify the behavioral and temperamental characteristics of dogs (Hsu & Serpell, 2003; McGreevy et al., 2013).

Owners are prompted to enter their dog’s body weight and breed as a part of the survey.

Although Dognition.com does collect data on dogs’ body weights, these values are entered in

10lb (4.6kg) increments limiting precision in estimating breed averages, particularly for small breeds.

Because the American Kennel Club (AKC) considers all poodles (Toy, Miniature, and

Standard) as one breed, Dognition.com does not distinguish between these morphs.

Consequently, there was large variation in the reported body weights of poodles in our sample.

From 10 to 70lbs, there were at least 10 individuals reported in each 10lb increment (n = 274 poodles in total). To more precisely model breed-typical brain weight within this sample, we split poodles into “miniature ” and “standard poodle” denominations based on body weights reported on Dognition.com. Using the C-BARQ database as a reference for the average weights of miniature poodles (mean = 15.47lbs, SD = 4.74lbs) and standard poodles (mean =

48.64lbs, SD = 15.43lbs), we grouped all poodles with a reported weight of 10 or 20lbs (n = 97) into the miniature poodle denomination, and all poodles with a reported weight greater than 40lbs (n = 155) into the standard poodle denomination. We excluded poodles with a reported weight of 30lbs (n = 22) because these values were intermediate to the two categories. Including these two poodle denominations, there were a total of 184 breeds in the Dognition.com database for which we were also able to obtain body weight data from the C-BARQ.

Validation of dog brain weight measures. To estimate brain weight for each breed in our sample, we used a brain weight-body weight scaling power function for dogs reported by

Bronson (1979), and validated this model using a sample of 24 breeds with known brain weights.

As a measure of breed-typical body weight, we used breed-mean body weights from the Canine

Behavioral Assessment and Research Questionnaire (C-BARQ) (Hsu & Serpell, 2003;

McGreevy et al., 2013). We excluded two breeds with brain weights reported in Bronson (1979) from our validation: toy poodle because we do not use this breed designation in our cognitive analyses, and standard because this was the only breed for which the body weight reported in (Bronson, 1979) (7.9kg) was more than two standard deviations smaller than the body weight reported on the C-BARQ (15.6kg).

The equation representing Bronson’s power function is y = 0.27x + 1.60, where ‘x’ is a base 10 logarithmic (log10) transformation of body weight in kilograms, and ‘y’ is a log10 transformation of brain weight in grams. Across 24 breeds with brain weights reported in

Bronson (1979), C-BARQ breed-mean body weight was a significant predictor of brain weight, β

= 0.28, t(22) = 14.71, p < .001, explaining 91% of the variance in brain weight (SE = 0.03; see

Figure S1). For the estimated brain weights of all 74 breeds in our sample, see Supplementary

Table 2.

To ensure that differences in shape between breeds did not cause systematic inaccuracies in our estimated brain weight values, we compiled cephalic index (CI) measurements from breeds reported in McGreevy et al. (2013) and Boyko et al. (2010). CI was calculated as maximum skull width multiplied by 100, and then divided by maximum skull length. There were 19 breeds which had both an observed brain weight reported in (Bronson,

1979) and a CI value reported in either McGreevy et al. (2013) or Boyko et al. (2010). Using k- means clustering to partition CI values from these breeds into both 2 and 3 clusters respectively, we observed no systematic overestimation or underestimation of brain weight based on CI in our sample, consistent with previous studies (Carreira, 2016).

Statistical Analysis. To control for genetic relatedness between breeds, the associations between estimated brain weight and cognitive measures were tested using Efficient Mixed

Modeling for Association studies (EMMA) (Kang et al., 2008; Zhou & Stephens, 2012). Genetic covariance between breeds was incorporated using a breed-average identity-by-state (IBS) matrix (Boyko et al., 2010), using molecular data from Hayward et al. (2016). Tests were conducted using the ‘EMMREML’ package (Akdemir & Godfrey, 2015) in the R environment

(v.3.3.1) (R Core Team, 2016). Relationships were considered significant at an alpha level of

0.05.

After filtering out the only breed included in our dataset for which no genetic data were available (miniature ), there were 7,397 individuals representing 74 breeds available for analyses (see Supplementary Table 2). Breeds with at least 20 individuals having completed any singular task were included in that task’s analyses regardless of how many individuals of that breed completed the other tasks. Average task performance by breed is shown in Supplementary Table 3.

Additional Results

Associations between brain size and cognition vary across cognitive domains. To explore whether behavioral data were stable across trials within tasks significantly associated with estimated brain weight and whether any variation over time differed as a function of estimated brain weight, we fit repeated measures mixed-models predicting task performance from trial number alone, as well as from a trial number by estimated brain weight interaction term. In Cunning, the Watching condition of Cunning alone, and Memory vs Pointing, trial number was a significant predictor of task performance (Cunning: β = -0.61, t(219) = -4.66, p <

0.001; [Cunning] Watching: β = -0.74, t(43) = -4.19, p < 0.001; Memory vs. Pointing: β = 0.001, t(179) = 2.46, p = 0.01). In the Watching condition of the Cunning task, dogs took significantly less time to pilfer the forbidden food over the course of the trials, while in Memory vs. Pointing, dogs became less likely to follow the pointing gesture over time. In Arm Pointing and the Not

Watching condition of Cunning alone, trial number was not a significant predictor of task performance (Arm Pointing: β = -0.00005, t(294) = -0.024, p = 0.98; [Cunning] Not Watching: β

= -0.29, t(131) = -1.29, p = 0.20). In no cases were there any significant trial number by estimated brain weight interactions (Arm Pointing: β = 0.00003, t(293) = 0.22, p = 0.83;

Cunning: β = 0.007, t(218) = 0.87, p = 0.38; [Cunning] Watching: β = 0.016, t(42) = 1.44, p =

0.16; [Cunning] Not Watching: β = -0.014, t(130) = -1.00, p = 0.32; Memory vs. Pointing: β =

0.0002, t(178) = 0.63, p = 0.53). The lack of significant interactions between trial number and brain weight demonstrates that while performance did vary as a function of trial number in three of the above measures, it did not vary differentially as a function of brain weight. We were unable to assess the potential for changes in performance due to learning across trials in the

Delayed Memory task, because each subsequent trial of this task is more difficult than the last (i.e. delay length increases with each trial), so performance is expected to vary as a function of trial number by design.

Body size. Comparisons of linear models predicting cognitive measures from breed- average body weight and estimated brain weight respectively revealed that for most measures in which performance was significantly associated with estimated brain weight in our main analyses, models predicting cognitive measures from estimated brain weight (Arm Pointing:

Adjusted R2 = 0.03, AIC = -201.86; Cunning: Adjusted R2 = 0.22, AIC = 221.48; Memory vs.

Pointing: Adjusted R2 = 0.08, AIC = -99.09; Delayed Memory: Adjusted R2 = 0.27, AIC = -

107.58) explained more of the variance in each cognitive measure and had a lower AIC than models predicting cognitive measures from body weight (Arm Pointing: Adjusted R2 = 0.02,

AIC = -201.24; Cunning: Adjusted R2 = 0.19, AIC = 223.42; Memory vs. Pointing: Adjusted R2

= 0.07, AIC = -98.79; Delayed Memory: Adjusted R2 = 0.24, AIC = -106.29). However, this was not true in all cases (Brain weight models -- [Cunning] Watching: Adjusted R2 = 0.17, AIC =

335.94; [Cunning] Not Watching: Adjusted R2 = 0.28, AIC = 334.14; Body weight models --

[Cunning] Watching: Adjusted R2 = 0.18, AIC = 335.22; [Cunning] Not Watching: Adjusted R2

= 0.28, AIC = 333.87), and differences in AIC and adjusted R2 were generally too small to draw meaningful conclusions about which models fit the cognitive data better. Results from mixed- models (controlling for genetic relatedness) predicting cognitive performance from CBARQ- reported breed-average body weight for each task within the same sample as our main breed- level analyses are presented in Supplementary Table 5, and corresponding plots are displayed in

Supplementary Figure 2.

Supplementary Table 1

Breed Body Weight (kg) Estimated Brain Weight (g) Age Male Female Airedale 25.74 ± 0.49 96.54 4.50 13 9 Akita 40.91 ± 0.65 109.64 4.43 11 15 38.42 ± 0.78 107.77 4.57 10 12 11.38 ± 0.41 77.15 7.55 16 14 American Terrier 26.29 ± 0.27 97.10 4.81 64 72 American Staffordshire 26.05 ± 0.46 96.86 Terrier 4.65 27 21 Australian Cattle Dog 19.72 ± 0.23 89.72 5.34 42 43 Australian Shepherd 20.52 ± 2.61 90.71 5.16 165 146 24.63 ± 0.62 95.38 5.87 21 12 12.79 ± 0.20 79.66 6.51 75 62 Belgian Malinois 26.83 ± 0.38 97.65 4.48 19 25 Bernese Mountain Dog 41.35 ± 0.50 109.97 4.34 28 17 Bichon Frise 6.78 ± 0.16 66.90 6.66 39 36 18.84 ± 0.15 88.60 5.33 191 163 Border Terrier 7.99 ± 0.26 69.98 5.57 21 15 9.41 ± 0.22 73.22 5.81 62 42 28.16 ± 0.33 98.95 5.19 101 72 Brittany 17.60 ± 0.31 86.96 5.02 25 27 24.08 ± 0.65 94.78 4.38 42 43 Cairn Terrier 7.64 ± 0.19 69.15 6.73 21 20 13.78 ± 0.45 81.30 5.99 11 12 Cavalier King Charles 7.99 ± 0.19 69.99 4.92 47 42 3.35 ± 0.07 55.10 5.96 75 85 Cocker Spaniel 11.72 ± 0.17 77.76 5.79 54 46 Collie 28.12 ± 0.38 98.91 5.43 21 28 Coton de Tulear 5.86 ± 0.41 64.28 5.11 19 19 7.20 ± 0.16 68.03 6.19 90 78 25.76 ± 0.47 96.56 5.57 11 17 Doberman Pinscher 33.77 ± 0.31 104.01 5.16 71 37 English Cocker Spaniel 12.93 ± 0.17 79.89 6.16 15 17 English Springer Spaniel 20.05 ± 0.26 90.13 5.61 64 48 Flat-Coated Retriever 28.81 ± 0.68 99.57 4.71 23 13 11.51 ± 0.24 77.38 4.46 53 41 Dog 34.50 ± 0.20 104.63 4.86 264 264 German Shorthaired Pointer 26.27 ± 0.52 97.08 5.94 30 21 Golden Retriever 31.04 ± 0.22 101.63 5.32 338 322 57.75 ± 0.80 120.54 5.15 24 25 30.89 ± 0.39 101.50 6.03 32 27 Havanese 5.72 ± 0.12 63.85 5.06 52 41 Irish Water Spaniel 27.81 ± 1.00 98.61 6.46 34 28 5.39 ± 0.22 62.83 5.87 14 10 Jack Russell Terrier 7.55 ± 0.13 68.92 6.39 45 41 31.59 ± 0.17 102.12 5.57 562 534 7.83 ± 0.26 69.61 5.60 13 8 Maltese 4.45 ± 0.13 59.58 7.17 39 35 5.28 ± 0.16 62.47 6.46 24 26 Miniature Poodle 7.02 ± 0.17 67.54 6.27 67 39 Miniature Schnauzer 7.89 ± 0.14 69.76 6.01 97 64 Newfoundland 57.39 ± 0.55 120.33 4.96 21 12 Papillon 3.97 ± 0.12 57.74 6.68 20 26 Parson Russell Terrier 7.55 ± 0.22 68.90 6.49 41 22 12.73 ± 0.23 79.55 5.18 50 37 Pomeranian 4.32 ± 0.14 59.11 5.78 38 31 Portuguese Water Dog 21.86 ± 0.37 92.29 5.40 38 31 8.79 ± 0.17 71.85 5.86 58 41 Rat Terrier 7.11 ± 0.22 67.79 7.19 24 23 Rhodesian Ridgeback 37.68 ± 0.43 107.20 4.41 35 31 42.02 ± 0.36 110.46 5.27 39 43 Samoyed 25.31 ± 0.80 96.09 4.88 12 13 10.48 ± 0.20 75.40 5.94 74 50 Shiba Inu 10.61 ± 0.18 75.67 5.34 29 20 6.28 ± 0.13 65.52 6.02 94 56 23.88 ± 0.34 94.56 5.33 41 47 Soft Coated Wheaten Terrier 16.42 ± 0.17 85.32 5.76 36 37 St. Bernard 59.75 ± 1.55 121.67 4.06 13 9 Staffordshire Bull Terrier 18.58 ± 0.42 88.26 5.75 17 20 Standard Poodle 22.06 ± 0.35 92.53 5.56 143 115 Standard Schnauzer 15.58 ± 0.56 84.09 5.39 18 14 Tibetan Terrier 10.73 ± 0.39 75.90 5.11 9 15 22.97 ± 0.42 93.57 5.28 42 32 30.71 ± 0.53 101.33 5.92 35 26 West Highland White Terrier 8.01 ± 0.17 70.04 6.29 37 38 14.20 ± 0.22 81.97 5.30 24 13 Yorkshire Terrier 3.72 ± 0.10 56.72 5.94 69 62

Supplementary Table 1. Mean body weight (± SEM, as reported on the C-BARQ), estimated brain weight, mean age, and sex breakdown for each of the 74 breeds that were included in our analyses. Average ages and sex breakdowns include all purebred dogs of each breed for which demographic information was submitted to Dognition.com, regardless of which cognitive tasks individuals completed. Supplementary Table 2

Breed Yawn Eye Arm Foot Cunn MvP MvS Mem IR PR 20 ------Akita 22 21 ------Alaskan Malamute 20 ------American Eskimo Dog 30 28 21 ------American Pit Bull Terrier 127 111 72 63 46 33 32 30 25 23 American Staffordshire Terrier 42 36 24 21 ------Australian Cattle Dog 79 71 45 42 33 29 27 27 21 21 Australian Shepherd 295 267 219 206 151 132 119 115 92 90 Basset Hound 26 24 ------Beagle 121 107 85 81 56 50 47 45 42 41 Belgian Malinois 42 37 31 28 ------Bernese Mountain Dog 42 36 26 26 ------Bichon Frise 67 62 37 33 23 - - - - - Border Collie 326 301 205 195 142 116 106 103 88 83 Border Terrier 33 30 23 22 ------Boston Terrier 92 83 55 54 35 20 20 20 - - Boxer 158 148 98 88 62 47 45 44 37 37 Brittany 49 42 31 29 22 20 - - - - Bulldog 84 72 48 43 30 22 20 20 - - Cairn Terrier 38 33 21 20 ------Cardigan Welsh Corgi 22 20 ------Cavalier 82 70 48 44 30 22 21 21 - - Chihuahua 141 120 70 68 44 33 30 29 23 23 Cocker Spaniel 90 77 50 44 33 27 25 25 21 21 Collie 48 42 31 30 23 20 - - - - Coton de Tulear 37 32 26 25 21 - - - - - Dachshund 158 136 82 77 51 42 40 36 29 29 Dalmatian 28 24 ------Doberman Pinscher 96 81 62 59 47 41 36 36 31 30 English Cocker Spaniel 30 22 ------English Springer Spaniel 108 93 68 66 41 33 32 31 26 24 Flat-Coated Retriever 35 33 23 22 ------French Bulldog 87 75 50 46 35 26 23 23 - - German Shepherd Dog 497 434 293 273 197 172 162 157 133 130 German Shorthaired Pointer 44 43 27 26 ------Golden Retriever 609 540 411 382 277 220 211 204 171 163 Great Dane 44 39 27 24 ------Greyhound 54 48 31 30 21 - - - - - Havanese 85 76 53 50 32 27 26 25 20 - Irish Water Spaniel 62 62 60 59 56 56 55 55 53 53 Italian Greyhound 22 ------Jack Russell Terrier 71 53 32 31 23 - - - - - Labrador Retriever 1021 909 657 613 479 408 378 365 306 293 Lhasa Apso 21 ------Maltese 69 61 32 27 ------Miniature Pinscher 46 39 27 26 20 - - - - - Miniature Poodle 96 87 57 57 45 43 39 36 31 31 Miniature Schnauzer 152 137 97 90 58 49 47 46 41 39 Newfoundland 32 26 ------Papillon 44 38 27 21 ------Parson Russell Terrier 59 52 31 30 ------Pembroke Welsh Corgi 83 71 54 53 42 36 35 35 28 28 Pomeranian 58 52 30 26 21 - - - - - Portuguese Water Dog 69 62 49 47 35 27 24 23 21 - Pug 89 77 48 42 29 25 25 25 21 20 Rat Terrier 43 38 22 21 ------Rhodesian Ridgeback 62 55 40 38 26 - - - - - Rottweiler 76 64 45 40 29 26 24 22 - - Samoyed 23 23 ------Shetland Sheepdog 117 107 76 74 60 52 51 51 41 39 Shiba Inu 47 44 26 26 ------Shih Tzu 135 116 75 66 42 35 34 34 25 22 Siberian Husky 81 74 51 48 29 29 26 24 24 24 Soft Coated Wheaten Terrier 67 60 46 42 32 28 26 25 - - St. Bernard 21 20 ------Staffordshire Bull Terrier 31 29 ------Standard Poodle 241 209 160 154 110 93 85 79 62 58 Standard Schnauzer 31 24 ------Tibetan Terrier 20 ------Vizsla 73 68 44 43 33 26 23 22 - - Weimaraner 55 52 35 33 24 - - - - - West Highland White Terrier 70 60 43 39 26 25 25 25 - - Whippet 35 30 20 20 ------Yorkshire Terrier 114 100 65 61 39 33 30 30 20 - Total 7344 6413 4342 4044 2710 2123 1949 1888 1432 1322

Supplementary Table 2. Number of individuals representing each of the 74 breeds included in each task in the cognitive analyses. Breeds with less than 20 individuals having completed a given task were excluded from that task’s analyses. Tasks are presented in order conducted from first to last, and are abbreviated as follows: Yawn = Yawning, Eye = Eye Contact, Arm = Arm Pointing, Foot = Foot Pointing, Cunn = Cunning, MvP = Memory vs. Pointing, MvS = Memory vs. Smell, Mem = Delayed Memory, IR = Inferential Reasoning, and PR = Physical Reasoning.

Supplementary Table 3

Breed Yawn Eye Arm Foot Cunn MvP MvS Mem IR PR Airedale Terrier -0.10 ± 0.12 ------Akita 0.09 ± 0.09 36.83 ± 4.50 ------Alaskan Malamute 0.10 ± 0.12 ------American Eskimo Dog 0.13 ± 0.10 52.36 ± 4.67 0.59 ± 0.05 ------American Pit Bull Terrier -0.04 ± 0.05 43.87 ± 2.24 0.67 ± 0.02 0.65 ± 0.03 -3.15 ± 2.12 0.70 ± 0.05 0.74 ± 0.05 0.84 ± 0.04 0.47 ± 0.05 0.59 ± 0.04 American Staffordshire Terrier 0.07 ± 0.08 45.44 ± 3.84 0.56 ± 0.03 0.59 ± 0.05 ------Australian Cattle Dog -0.05 ± 0.06 50.75 ± 2.82 0.66 ± 0.03 0.64 ± 0.04 -3.86 ± 2.89 0.69 ± 0.06 0.72 ± 0.04 0.81 ± 0.04 0.43 ± 0.04 0.64 ± 0.04 Australian Shepherd 0.00 ± 0.03 57.29 ± 1.51 0.69 ± 0.01 0.67 ± 0.01 0.30 ± 1.38 0.71 ± 0.03 0.74 ± 0.02 0.83 ± 0.02 0.50 ± 0.02 0.60 ± 0.02 Basset Hound 0.04 ± 0.13 50.04 ± 5.52 ------Beagle -0.02 ± 0.05 56.22 ± 2.50 0.63 ± 0.02 0.63 ± 0.02 3.09 ± 1.88 0.73 ± 0.03 0.81 ± 0.03 0.82 ± 0.03 0.46 ± 0.04 0.60 ± 0.04 Belgian Malinois 0.12 ± 0.11 58.84 ± 3.95 0.68 ± 0.04 0.70 ± 0.03 ------Bernese Mountain Dog 0.02 ± 0.09 50.04 ± 4.09 0.76 ± 0.04 0.71 ± 0.05 ------Bichon Frise -0.03 ± 0.05 50.28 ± 3.21 0.64 ± 0.03 0.67 ± 0.04 2.84 ± 5.04 - - - - - Border Collie 0.02 ± 0.03 46.60 ± 1.43 0.69 ± 0.02 0.67 ± 0.02 -0.13 ± 1.38 0.62 ± 0.03 0.72 ± 0.03 0.80 ± 0.02 0.46 ± 0.03 0.66 ± 0.03 Border Terrier 0.03 ± 0.08 59.44 ± 5.08 0.65 ± 0.04 0.69 ± 0.04 ------Boston Terrier -0.05 ± 0.05 60.01 ± 2.91 0.60 ± 0.03 0.60 ± 0.03 1.74 ± 3.55 0.71 ± 0.06 0.79 ± 0.05 0.79 ± 0.06 - - Boxer -0.01 ± 0.04 58.63 ± 2.05 0.65 ± 0.02 0.66 ± 0.02 -0.42 ± 2.49 0.57 ± 0.05 0.75 ± 0.04 0.73 ± 0.04 0.43 ± 0.04 0.55 ± 0.05 Brittany 0.08 ± 0.08 62.14 ± 4.23 0.66 ± 0.04 0.63 ± 0.03 0.48 ± 3.27 0.69 ± 0.07 - - - - Bulldog -0.11 ± 0.06 46.32 ± 3.00 0.68 ± 0.03 0.64 ± 0.04 4.53 ± 1.85 0.63 ± 0.07 0.68 ± 0.07 0.80 ± 0.05 - - Cairn Terrier -0.11 ± 0.09 53.53 ± 3.84 0.57 ± 0.05 0.67 ± 0.05 ------Cardigan Welsh Corgi 0.05 ± 0.14 38.83 ± 5.03 ------Cavalier King Charles Spaniel 0.01 ± 0.06 60.24 ± 3.14 0.66 ± 0.02 0.69 ± 0.03 -0.41 ± 3.02 0.56 ± 0.07 0.67 ± 0.08 0.69 ± 0.06 - - Chihuahua -0.01 ± 0.04 42.45 ± 2.34 0.65 ± 0.03 0.59 ± 0.03 -0.01 ± 2.94 0.70 ± 0.06 0.72 ± 0.06 0.77 ± 0.05 0.42 ± 0.06 0.63 ± 0.04 Cocker Spaniel -0.01 ± 0.06 58.81 ± 2.97 0.65 ± 0.03 0.66 ± 0.03 2.52 ± 3.13 0.60 ± 0.07 0.79 ± 0.05 0.77 ± 0.05 0.46 ± 0.06 0.67 ± 0.05 Collie 0.04 ± 0.08 52.18 ± 4.09 0.61 ± 0.04 0.61 ± 0.04 3.02 ± 3.22 0.69 ± 0.08 - - - - Coton de Tulear 0.11 ± 0.08 54.89 ± 3.86 0.62 ± 0.03 0.60 ± 0.04 0.57 ± 3.92 - - - - - Dachshund 0.01 ± 0.04 55.17 ± 2.10 0.63 ± 0.02 0.62 ± 0.02 3.11 ± 2.87 0.64 ± 0.05 0.79 ± 0.04 0.81 ± 0.04 0.39 ± 0.05 0.58 ± 0.05 Dalmatian 0.00 ± 0.09 45.29 ± 5.02 ------Doberman Pinscher 0.04 ± 0.06 51.26 ± 2.72 0.71 ± 0.03 0.66 ± 0.03 1.87 ± 2.76 0.59 ± 0.05 0.66 ± 0.04 0.78 ± 0.04 0.42 ± 0.05 0.52 ± 0.03 English Cocker Spaniel -0.17 ± 0.12 63.06 ± 5.24 ------English Springer Spaniel 0.04 ± 0.05 64.22 ± 2.41 0.73 ± 0.03 0.70 ± 0.03 -1.55 ± 2.37 0.62 ± 0.06 0.71 ± 0.05 0.84 ± 0.03 0.42 ± 0.06 0.55 ± 0.05 Flat-Coated Retriever -0.09 ± 0.10 64.79 ± 4.16 0.67 ± 0.05 0.66 ± 0.05 ------French Bulldog -0.01 ± 0.05 50.48 ± 2.80 0.59 ± 0.03 0.64 ± 0.04 1.80 ± 2.07 0.68 ± 0.05 0.78 ± 0.05 0.76 ± 0.05 - - German Shepherd Dog -0.03 ± 0.02 46.60 ± 1.21 0.67 ± 0.01 0.64 ± 0.01 -0.96 ± 1.31 0.68 ± 0.02 0.72 ± 0.02 0.80 ± 0.02 0.51 ± 0.02 0.62 ± 0.02 German Shorthaired Pointer -0.05 ± 0.09 46.13 ± 3.53 0.65 ± 0.03 0.62 ± 0.04 ------Golden Retriever 0.02 ± 0.02 57.57 ± 1.08 0.67 ± 0.01 0.65 ± 0.01 -0.52 ± 1.19 0.62 ± 0.02 0.76 ± 0.02 0.80 ± 0.02 0.44 ± 0.02 0.65 ± 0.02 Great Dane -0.02 ± 0.10 45.30 ± 3.56 0.60 ± 0.04 0.60 ± 0.04 ------Greyhound 0.02 ± 0.06 31.43 ± 3.17 0.56 ± 0.04 0.49 ± 0.03 -4.71 ± 3.60 - - - - - Havanese 0.01 ± 0.06 52.14 ± 2.71 0.66 ± 0.03 0.63 ± 0.03 8.16 ± 3.81 0.72 ± 0.06 0.77 ± 0.05 0.69 ± 0.06 0.40 ± 0.05 - Irish Water Spaniel -0.05 ± 0.06 65.60 ± 2.98 0.72 ± 0.03 0.71 ± 0.03 -0.20 ± 2.91 0.55 ± 0.05 0.63 ± 0.04 0.89 ± 0.03 0.52 ± 0.03 0.68 ± 0.03 Italian Greyhound 0.14 ± 0.12 ------Jack Russell Terrier 0.06 ± 0.05 44.62 ± 3.67 0.61 ± 0.03 0.63 ± 0.04 -1.77 ± 3.55 - - - - - Labrador Retriever 0.04 ± 0.02 55.28 ± 0.83 0.67 ± 0.01 0.64 ± 0.01 -0.92 ± 0.75 0.63 ± 0.02 0.77 ± 0.01 0.81 ± 0.01 0.46 ± 0.01 0.61 ± 0.01 Lhasa Apso -0.14 ± 0.10 ------Maltese 0.07 ± 0.07 45.74 ± 3.26 0.62 ± 0.03 0.62 ± 0.04 ------Miniature Pinscher 0.00 ± 0.08 51.14 ± 3.67 0.59 ± 0.05 0.67 ± 0.05 5.38 ± 5.34 - - - - - Miniature Poodle 0.03 ± 0.05 56.72 ± 2.84 0.65 ± 0.03 0.64 ± 0.03 5.45 ± 2.87 0.74 ± 0.04 0.81 ± 0.04 0.76 ± 0.05 0.42 ± 0.05 0.58 ± 0.04 Miniature Schnauzer 0.01 ± 0.04 51.55 ± 2.23 0.66 ± 0.02 0.66 ± 0.02 -1.69 ± 2.34 0.68 ± 0.05 0.78 ± 0.03 0.85 ± 0.03 0.40 ± 0.04 0.61 ± 0.04 Newfoundland -0.12 ± 0.11 50.97 ± 4.88 ------Papillon 0.00 ± 0.07 50.87 ± 4.53 0.67 ± 0.04 0.74 ± 0.05 ------Parson Russell Terrier 0.14 ± 0.06 53.42 ± 3.96 0.73 ± 0.04 0.69 ± 0.04 ------Pembroke Welsh Corgi 0.06 ± 0.06 48.83 ± 2.98 0.65 ± 0.03 0.62 ± 0.03 0.89 ± 3.31 0.75 ± 0.05 0.76 ± 0.04 0.79 ± 0.05 0.40 ± 0.05 0.68 ± 0.05 Pomeranian 0.02 ± 0.07 51.36 ± 3.82 0.61 ± 0.04 0.65 ± 0.03 8.30 ± 4.40 - - - - - Portuguese Water Dog 0.01 ± 0.07 59.71 ± 2.77 0.64 ± 0.03 0.57 ± 0.03 -1.59 ± 3.33 0.64 ± 0.06 0.73 ± 0.05 0.84 ± 0.05 0.44 ± 0.04 - Pug 0.01 ± 0.05 59.00 ± 2.70 0.67 ± 0.03 0.69 ± 0.03 8.65 ± 3.23 0.63 ± 0.06 0.72 ± 0.04 0.74 ± 0.05 0.51 ± 0.05 0.52 ± 0.06 Rat Terrier 0.16 ± 0.07 54.55 ± 4.38 0.69 ± 0.05 0.62 ± 0.06 ------Rhodesian Ridgeback 0.03 ± 0.06 46.10 ± 3.49 0.68 ± 0.03 0.61 ± 0.04 -1.04 ± 4.72 - - - - - Rottweiler 0.01 ± 0.08 54.97 ± 3.37 0.65 ± 0.03 0.70 ± 0.03 3.70 ± 3.22 0.69 ± 0.06 0.73 ± 0.07 0.83 ± 0.05 - - Samoyed -0.04 ± 0.13 44.00 ± 5.56 ------Shetland Sheepdog 0.02 ± 0.05 54.05 ± 2.64 0.65 ± 0.02 0.62 ± 0.03 -0.03 ± 2.33 0.70 ± 0.05 0.67 ± 0.04 0.71 ± 0.04 0.51 ± 0.04 0.58 ± 0.03 Shiba Inu -0.02 ± 0.06 38.28 ± 3.27 0.57 ± 0.05 0.70 ± 0.04 ------Shih Tzu -0.04 ± 0.04 45.75 ± 2.40 0.63 ± 0.03 0.62 ± 0.03 5.06 ± 2.57 0.60 ± 0.05 0.64 ± 0.06 0.71 ± 0.06 0.47 ± 0.06 0.51 ± 0.06 Siberian Husky 0.09 ± 0.07 41.42 ± 2.68 0.62 ± 0.03 0.64 ± 0.03 0.36 ± 3.24 0.68 ± 0.06 0.79 ± 0.05 0.82 ± 0.05 0.44 ± 0.04 0.54 ± 0.05 Soft Coated Wheaten Terrier -0.07 ± 0.07 54.68 ± 3.43 0.61 ± 0.03 0.59 ± 0.04 1.44 ± 4.13 0.68 ± 0.06 0.72 ± 0.05 0.66 ± 0.06 - - St. Bernard 0.00 ± 0.14 53.10 ± 5.57 ------Staffordshire Bull Terrier 0.13 ± 0.11 47.02 ± 4.10 ------Standard Poodle 0.03 ± 0.03 58.64 ± 1.78 0.67 ± 0.02 0.64 ± 0.02 1.77 ± 1.71 0.69 ± 0.03 0.72 ± 0.03 0.78 ± 0.03 0.50 ± 0.03 0.63 ± 0.03 Standard Schnauzer 0.00 ± 0.08 50.86 ± 5.49 ------Tibetan Terrier 0.15 ± 0.13 ------Vizsla 0.12 ± 0.06 59.86 ± 2.93 0.72 ± 0.03 0.61 ± 0.04 4.60 ± 2.76 0.50 ± 0.08 0.75 ± 0.06 0.76 ± 0.06 - - Weimaraner -0.04 ± 0.08 50.07 ± 3.86 0.58 ± 0.03 0.66 ± 0.04 -5.62 ± 4.12 - - - - - West Highland White Terrier 0.04 ± 0.06 43.22 ± 2.89 0.64 ± 0.04 0.62 ± 0.04 3.51 ± 3.96 0.75 ± 0.05 0.65 ± 0.07 0.71 ± 0.06 - - Whippet 0.00 ± 0.10 48.69 ± 3.91 0.67 ± 0.05 0.59 ± 0.05 ------Yorkshire Terrier 0.09 ± 0.05 49.63 ± 2.66 0.62 ± 0.03 0.65 ± 0.03 4.56 ± 2.75 0.72 ± 0.05 0.69 ± 0.04 0.68 ± 0.05 0.59 ± 0.07 -

Supplementary Table 3. Mean score (± SEM) on each task for all breeds included in the cognitive analyses. Tasks are presented in order conducted from first to last, and are abbreviated as follows: Yawn = Yawning, Eye = Eye Contact, Arm = Arm Pointing, Foot = Foot Pointing, Cunn = Cunning, MvP = Memory vs. Pointing, MvS = Memory vs. Smell, Mem = Delayed Memory, IR = Inferential Reasoning, and PR = Physical Reasoning. Scores on each task were calculated as follows: Yawn = Binary measure (at least one yawn or no yawns) in test condition minus control condition; Eye = Duration of eye contact in seconds; Arm and Foot = Proportion of gesture follows; Cunn = Seconds to take food in the Watching condition minus the Not Watching condition; MvP and MvS = Proportion of searches to remembered location; Mem, IR, and PR = Proportion of successful searches.

Supplementary Table 4

Task n β χ2 p Yawning 7285 -0.00014 0.13 0.72 Eye Contact 6448 0.017 0.12 0.73 Arm Pointing 4510 0.00068 6.51 0.011* Foot Pointing 4215 0.00004 0.02 0.89 Cunning 3045 -0.080 13.40 <0.001* Watching Condition 3046 0.27 10.25 0.001* Not Watching Condition 3097 0.33 15.34 <0.001* Memory vs. Pointing 2548 -0.0011 3.64 0.056 Memory vs. Smell 2390 0.00010 0.05 0.83 Delayed Memory 2310 0.0015 11.06 <0.001* Inferential Reasoning 1924 0.00084 3.70 0.054 Physical Reasoning 1852 0.00092 4.00 0.045*

Supplementary Table 4. Results from mixed linear models (controlling for breed-level genetic relatedness) predicting cognitive performance from breed-average estimated brain weight for each task on an individual level. Significant p-values are denoted in bold.

Supplementary Table 5 Task β χ2 p Yawning -0.00072 1.37 0.24 Eye Contact -0.043 0.44 0.51 Arm Pointing 0.00083 3.35 0.07 Foot Pointing -0.00014 0.09 0.78 Cunning -0.14 10.77 0.001* Watching Condition 0.49 10.78 0.001* Not Watching Condition 0.63 18.21 <0.001* Memory vs. Pointing -0.002 3.67 0.06 Memory vs. Smell -0.0005 0.35 0.56 Delayed Memory 0.0028 12.10 <0.001* Inferential Reasoning 0.0003 0.10 0.75 Physical Reasoning 0.00048 0.18 0.67 Supplementary Table 5. Results from mixed linear models (controlling for genetic relatedness) predicting cognitive performance from CBARQ- reported breed-average body weight for each task within the same sample as our main breed-level analyses (Table 1). Significant p-values are denoted in bold.

Supplementary Figure 1

Supplementary Figure 1. Plot of log10 transformed C-BARQ breed- average body weights (in kilograms) and brain weights (in grams) reported in Bronson (1979) for 24 breeds with a linear model predicting brain weight from body weight overlaid. Supplementary Figure 2

Supplementary Figure 2. Scores on all cognitive tasks a function of CBARQ-reported breed-average body weight across dog breeds. The dashed lines show the regression slopes from statistical models controlling for genetic relatedness between breeds. Each breed included in the analyses had at least 20 individuals complete a given task, and is represented by one diamond. Supplementary References

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