Peer review of: Behavioural correlations of the domestication syndrome are decoupled in modern dog (2019)

Reviewers' Comments:  
 
Reviewer #1:  
Remarks to the Author:  
The Authors investigate if phenotypic correlations (inferred as between-individual correlations) among 
suites of behavioral traits are different between ancient and modern breeds. Their main hypothesis is 
that these traits will generally correlate with each other as a consequence of correlated response to 
selection (domestication syndrome hypothesis). However, they show that this prediction is more likely 
to hold for ancient breeds, while modern breeds can be characterized by weaker correlations resulting 
from the decoupled evolution of behaviors during the latter phases of the domestication process.  
 
Although I am not an expert on dog evolution (and on any dog-related topic) and domestication, I 
assume that the evidence for the independent evolution of originally linked phenotypic traits in 
relation to domestication is an important novelty component, and I read the paper with great interest. 
I note however that idea of the “braking down” of behavioral correlations under certain environmental 
conditions or selection regimes is well known, and research has shown analogue patterns in response 
to urbanization for example (i.e. behaviors that correlate in natural habitats may no longer show 
correlation in an urban habitat). Hence, for the wider-scale interpretation of the results, it would be 
straightforward to point to the general hypothetical/empirical background from the behavioral 
syndrome literature (e.g. dating back to Andy Sih's great reviews).  

I can identify two aspects of the presented data that remained unexplored in the given context. First, I 
was wondering what the Authors’ would predict/detect for the correlation of behavioral traits at the 
among-breed level (correlations among the breed-specific mean scores). If the link between 
behavioral traits is decupled because there is a selection on one behavioral trait but not on others, this 
would target breed-specific mean values differently which can have consequences for the among-
breed correlation as well. Are there differences between modern and ancient breeds in this regard as 
well?  
 
Although it is evident that some of the within-breed correlations are smaller in the modern than in the 
ancient breeds, the effect sizes are strongly correlated across the two categories (r = 0.83 based on 
the data presented in Table 1, see a figure attached). If domestication depletes most of the behavioral 
correlations in modern breeds, I would predict much weaker correlation between the two sets of effect 
sizes. Without this I cannot exclude that most of the statistical difference found between particular 
pairs of effects sizes (on Fig 1) is due to the fact that modern breeds correspond to extremely large 
sample sizes (both in terms of number of individuals and number of breeds) and the errors around 
these estimates are very small (see further comments along this line below).  
 

 

 
I would have further advises along which the Authors could improve their statistics:  
 
1) The main conclusions of the study rely on models in which both breed category (modern vs. 
ancient) and distance to wolf (“non-independence” of breeds) are simultaneously entered as fixed 
predictors. These two variables are heavily confounded by definition (i.e. modern breeds are 
necessarily at higher distance from wolf) that calls for issues about collineairity. When predictors are 
strongly associated it is impossible to determine their partial explanatory power from a model that 
includes both. Therefore, it remains difficult to tease apart whether the modern-ancient distinction at a 
broad scale, or the common ancestry at a finer scale that is responsible for the among-breed variation 
in effect sizes. I do not think that this is a crucial problem for the Authors’ main conclusion, but some 
clarifications and more careful interpretation might be needed. Furthermore, the proper “phylogenetic” 
control is not necessarily achieved by the above model using distance to wolf as a fixed predictor, but 
such effects should be preferably entered to define the residual structure (i.e. phylogenetic least 
square methods) or as a random effect (phylogenetic mixed model). Based on these phylogenetic 
approaches, the Authors could test the phylogenetic signal in the data, which could even be done 
separately for ancient and modern dog breeds allowing the separation of the category/relatedness 
effects.  
 
2) It is assumed that age- sex- and observer effects are unlikely to pose problems in the analyses. 
However, given the much smaller sample sizes for ancient breeds than that of modern breeds, biased 
sampling can easily occur by chance. For example, due to owners’ behavior some ancient breeds 
might be tested at somewhat different ages than some the grand average of the individuals from 
modern breeds, or they might be evaluated by a smaller subset of observers. This is an empirical 
question, and instead of relying on pure assumptions for unbiased sampling, it would be more 

convincing if the within-breed (and potentially the between-breed) correlations could be obtained from 
a mixed linear model including all individuals, in which age- and sex- effects are controlled for (as 
fixed effects), and the hierarchical structure is handled through the random effect structure (breed 
and observer ID). Additionally, the relatedness matrix of breeds could also be considered in this 
model.  
 
3) A bootstrap exercise is performed in order to verify that the vast sample size difference between 
breed categories is unlikely to confound the main results. This is a good strategy, but unfortunately 
the bootstrap only considers differences in terms of the number of individuals. Ideally, one could also 
set up a regime for the random sampling, in which only 7 breeds are sampled (randomly) from the 
modern breeds. In this way, the sample sizes would become more balanced.  
 
4) The Authors use the functions available from the nlme() package to perform meta-analyses. 
However, this package has not been developed for meta-analyses. The models fitted by the nlme() 
function particularly assume that the sampling variances are known only up to a proportionality 
constant. This is not what meta-analytic models do, as they specifically assume that the sampling 
variances are known. See http://www.metafor-project.org/doku.php/tips:rma_vs_lm_lme_lmer. I 
suggest using the metafor() or MCMCglmm() packages that can appropriately perform meta-analyses 
(and can also handle “phylogenetic effects” and account for the hierarchical structure of data)  
 
 
The paper reads very well, but the supporting material contains several leftovers potentially from 
earlier versions that make interpretations difficult at some places.  
 
 
 
Reviewer #2:  
Remarks to the Author:  
This is an interesting manuscript dealing with the evolution of behavioral correlations during 
domestication. Differences in correlation structure among types of breeding (ancient vs. modern) 
imply the existence of relative rather than absolute constraints on the evolution of behavioral 
architecture and is of great interest as such, though this aspects if not highlighted in the paper. 
Multivariate approaches to the data analyses should be applied to understand whether changes in 
variance rather than trait integration caused these effects. However, as the study does not address 
genetic variances and covariances directly, there are multiple competing explanations for the results, 
namely differences in heritability between types, and differences in non-genetic correlations between 
types causing the reported effects, firm conclusions cannot be drawn.  
 
Introduction  
 
Line 53. Linkage disequilibrium should also be mentioned as a valid explanation. For a good example 
in the context of among-species differentiation, see Beldade et al. 2002 PNAS.  
 
Line 83-87. I do not understand the rational for the hypothesized directions: Why should aggressive 
animals be more fearful when a pleiotropic genetic or hormonal mechanism is implied?  
 
Line 87-88. It would be useful to introduce correlational selection as an explanation for the behavioral 
correlations described in lines 84-87, rather than just mentioning proximate mechanisms (line 83-
84).  
 
Line 87. The hypothesis posited here is too phenomenological for my taste. Please introduce an 

adaptive argument explaining why correlational selection pressures affecting trait integration would 
have changed.  
 
Line 92-93. Perhaps it would be more useful to rephrase such texts to talk about absolute versus 
relative constraints on the adaptive evolution of behavior, this study representing evidence supporting 
the latter explanation. See the Beldade et al. 2002 paper mentioned above.  
 
Line 118. Based on each dog assayed once?  
 
Line 129-onwards (Results). Three key issues obstruct a firm interpretation of the results:  
 
1. Changes in correlations are often due to changes in variance. Here, the lower correlations in 
modern breeds could be caused by a reduction in variance in modern breeds. Authors should therefore 
also estimate differences in the variance-covariance matrix rather than focusing on correlations alone.  
 
2. Spearman rank correlations should best not be used as non-parametric stats do not connect well 
with multivariate evolutionary theory tested here.  
 
3. There is no reason to focus on 17 pairs of bivariate correlations in isolation. Evolutionary biologists 
have developed methods to compare multivariate variance-covariance and correlations matrices from 
which information can be derived equivalent to what the authors are interested in here (e.g. 
evolutionary autonomy measures, see Dochtermann & Dingemanse 2013 for an application to 
behavioral syndrome research). I strongly suggest that the overall interpretation and conclusions are 
based on analyzing differences in aspects of the multivariate correlation matrix  
 
Line 246-onwards (Discussion). The phenotypic correlation (rP) between two traits equals the genetic 
correlation (rG) times the geometric mean heritability of the two traits plus the environmental 
correlation (rE) times (1 – the geometric mean heritability) (see Roff 1997 Evolutionary Quantitative 
Genetics). The authors largely imply that the weaker phenotypic correlations observed in the modern 
breeds are due to weaker genetic correlation structures, but as the equation shows, there are two 
alternative explanations:  
 
1. Genetic and environmental correlations often differ (e.g. this is why G and P matrices differ 
somewhat in Dochtermann's 2011 Evolution paper on behavioral syndromes) even if both don’t differ 
between the types of breed. If so (i.e., rG <> rE), differences between ancient and modern breeds in 
geometric mean heritability will cause differences in phenotypic correlations observed here despite the 
two types not differing in the tightness of the genetic integration of behaviors. A discussion about 
breed-type specific heritability is thus required. The conclusions should be toned down. In short, this is 
not sufficient evidence that trait integration has loosened.  
 
Second, genetic correlations indicative of genetic integration of the behaviors might be the same for 
the two types of breed but environmental correlations (i.e., due to developmental plasticity) might 
differ between modern and ancient breeds. Those environmental correlations occur when the same 
environmental factor has pleiotropic effects on multiple traits. It is very likely that ancient and modern 
breeds experience very different environments (because of how they are used by their owners, and 
raised by breeders), hence differences in the phenotypic correlations reported here might simply 
emerge from differences in environmental conditions that the two breed types currently experience. 
Again, as discussion is required, and conclusions should be toned down, as this mechanism may imply 
that the conclusions currently drawn may be invalid.  
 
01/03/2018, Signed, Niels Dingemanse  

 
 
 
Reviewer #3:  
Remarks to the Author:  
This is a very interesting and original paper.  
 
The authors attempt to use a remarkably large database on dog behavior to test for behavioral 
correlations predicted by the "domestication syndrome." Specifically, they tested whether sociability 
was correlated with playfulness and aggression with fearfulness. The results were not supported in 
modern breeds, but were supported in ancient breeds. They use these findings to argue that the 
domestication syndrome can become uncoupled so that domestication-related behaviors become 
independently selected for in modern dogs.  
I think this is a very exciting and important paper. I hope it can be published, but I have a few 
questions I would like to see cleared up before giving my endorsement.  
 
The use of the Working Dog Mentality Assessment (DMA) of the Swedish working dog association 
(SWDA) provides access to an immense (in this paper now 90,000 dog) behavioral database. For 
direct behavioral testing of a mammal this is a totally unprecedented scale, and much is gained by 
using it. But it needs to be kept in mind that, although the test is administered with great seriousness 
by the SWDA, it was not developed by scientists. Previous studies have, as cited in the paper, 
provided some evidence of validity for it, but there are nonetheless issues around using a non-
scientific instrument that are not removed by the sheer number of animals tested. The DMA is carried 
out outdoors at sites throughout Sweden by a vast number of trained test-givers (I believe many 
hundreds, perhaps thousands). Given that the outcome of interest in this paper lies in a comparison of 
modern breeds to ancient breeds, we need to consider that the modern and ancient breeds may not 
have been assigned at random to different test-givers and locales. Is it not possible that certain 
breeds of dogs are more commonly found in the North of Sweden and others in the South, or some in 
the country and others in the city, and thus may be tested in locations and by test-givers that lead to 
different criteria, and that this could influence the outcome? This should be addressed. (I thought 
there was a study by Svartberg which reported that the single largest factor in a factor analysis of 
scores from the DMA was the identity of the individual carrying out the test, but I cannot now find that 
study so maybe I'm wrong about that.)  
 
The Intro fails to explain why the particular patterns of correlation (sociability with playfulness and 
aggression with fearfulness) are expected.  
 
What is the evidence that the dogs are truly of the breeds claimed? It appears to be owner report: If 
so, what is the basis for believing these reports? Or did the dogs have breed-club papers, or DNA 
tests?