The mark of captivity: plastic responses in the ankle bone of a wild ungulate (Sus scrofa)

Deciphering the plastic (non-heritable) changes induced by human control over wild animals in the archaeological record is challenging. We hypothesized that changes in locomotor behaviour in a wild ungulate due to mobility control could be quantified in the bone anatomy. To test this, we experimented with the effect of mobility reduction on the skeleton of wild boar (Sus scrofa), using the calcaneus shape as a possible phenotypic marker. We first assessed differences in shape variation and covariation in captive-reared and wild-caught wild boars, taking into account differences in sex, body mass, available space for movement and muscle force. This plastic signal was then contrasted with the phenotypic changes induced by selective breeding in domestic pigs. We found that mobility reduction induces a plastic response beyond the shape variation of wild boars in their natural habitat, associated with a reduction in the range of locomotor behaviours and muscle loads. This plastic signal of captivity in the calcaneus shape differs from the main changes induced by selective breeding for larger muscle and earlier development that impacted the pigs' calcaneus shape in a much greater extent than the mobility reduction during the domestication process of their wild ancestors.

I have only one, minor and rather semantic comment, that I think should be considered by the authors when revising the manuscript.This concerns only the theoretical framing of the experiment. In the introduction, second paragraph I urge the authors to revisit their use of "domestication syndrome" (lines 52-58). Recent re-evaluation of the concept by Lord et al. (in press, CellPress Reviews) has called into question the ubiquity and indeed the utility of the domestication syndrome trait-package. While the nature of the experiment makes it clear that the authors of this manuscript in review are not limiting their study of domestication to the narrow genetic confines imposed by reliance on this trait package, by stating they are "all shared among domestic species, regardless of their phylogenetic relationships" they seem to reify it. The problem with the domestication syndrome is less that the traits associated with it are "questionable for tracking early domestication"--although this is certainly true as well--but more that such traits have been long assumed as universal markers at all. As phrased, the use of the domestication syndrome as a means to highlight the dearth of attention that plastic responses and selective contexts have received comes off as a bit of a straw man. A more nuanced treatment that at minimum gives a nod to the controversy and debate surrounding the validity of such a syndrome is needed here.

Review form: Reviewer 2
Is the manuscript scientifically sound in its present form? Yes

Are the interpretations and conclusions justified by the results? Yes
Is the language acceptable? Yes

Do you have any ethical concerns with this paper? No
Have you any concerns about statistical analyses in this paper? No Accept with minor revision (please list in comments)

Comments to the Author(s)
I have a few observations which the authors could consider addressing in the paper if appropriate. 1) One of their wild caught boar samples appears to have came from the same reserve (Urciers) as their experimental animals. This is very important in validating the actual experiment (i.e. the only wild-caught control for environment, altitude,vegetaion etc) but not really highlighted enough in the text. 2) Following on from 1), the wild caught boar from other parts of France and Switzerland were likely from different environments etc, but all the data is pooled (understandably) when comparing with experimental and domestic data. I know the sample sizes are small, but were there any differences in shape between these different wild boar populations?
3) It's interesting that the Corsican free-range pigs are at the extreme end of shape divergence (Fig  6a). Not much further is said about this. Not what I would have expected, so what might be the explanation? 4) I'm intrigued by the counter-intuitive (but well-explained in the paper) discussion about reduced mobility and additional increased muscle forces, along with no evidence for size decrease in captivity -but likely an initial increase). Does this perhaps support/explain evidence presented by others using GMM approaches to explore pig domestication, who have claimed the presence of a 'domestic' tooth shape in early Neolithic suids associated with large sized animals indistinguishable in size to wild boar?

Dear Dr Cucchi
On behalf of the Editors, I am pleased to inform you that your Manuscript RSOS-192039 entitled "The mark of captivity: plastic responses in the ankle bone of a wild ungulate (Sus scrofa)" has been accepted for publication in Royal Society Open Science subject to minor revision in accordance with the referee suggestions. Please find the referees' comments at the end of this email.
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Once again, thank you for submitting your manuscript to Royal Society Open Science and I look forward to receiving your revision. If you have any questions at all, please do not hesitate to get in touch. Comments to the Author(s) This paper represents an important contribution to the study of domestication as an evolutionary process. It provides a powerful new methodological tool that has the potential to re-orient our understanding of the process of domestication from the biological results, to the behavioral impetus. The authors succeed in providing credible evidence for plastic responses in the skeletal morphology of S. scrofa resulting from human-driven changes in locomotor behaviour. By focusing on and providing evidence for the effects of confinement on wild populations--likely one of the earliest human behaviors driving the evolutionary transition we recognize as domestication--this paper not only provides a specific and powerful new tool for identifying one form of early human intervention setting the stage for evolutionary change, but it also provides a model for archaeologists and other researchers interested in domestication for studies that more closely account for how context and contingency structure both the process itself and its outcome, which has historically received insufficient attention. I commend the authors for the scientifically sound and forward-thinking research design they present here, and am convinced and thrilled by their results. Therefore, it is with great enthusiasm that I recommend this paper for publication.
I have only one, minor and rather semantic comment, that I think should be considered by the authors when revising the manuscript.This concerns only the theoretical framing of the experiment. In the introduction, second paragraph I urge the authors to revisit their use of "domestication syndrome" (lines 52-58). Recent re-evaluation of the concept by Lord et al. (in press, CellPress Reviews) has called into question the ubiquity and indeed the utility of the domestication syndrome trait-package. While the nature of the experiment makes it clear that the authors of this manuscript in review are not limiting their study of domestication to the narrow genetic confines imposed by reliance on this trait package, by stating they are "all shared among domestic species, regardless of their phylogenetic relationships" they seem to reify it. The problem with the domestication syndrome is less that the traits associated with it are "questionable for tracking early domestication"--although this is certainly true as well--but more that such traits have been long assumed as universal markers at all. As phrased, the use of the domestication syndrome as a means to highlight the dearth of attention that plastic responses and selective contexts have received comes off as a bit of a straw man. A more nuanced treatment that at minimum gives a nod to the controversy and debate surrounding the validity of such a syndrome is needed here.

Reviewer: 2
Comments to the Author(s) I have a few observations which the authors could consider addressing in the paper if appropriate. 1) One of their wild caught boar samples appears to have came from the same reserve (Urciers) as their experimental animals. This is very important in validating the actual experiment (i.e. the only wild-caught control for environment, altitude,vegetaion etc) but not really highlighted enough in the text. 2) Following on from 1), the wild caught boar from other parts of France and Switzerland were likely from different environments etc, but all the data is pooled (understandably) when comparing with experimental and domestic data. I know the sample sizes are small, but were there any differences in shape between these different wild boar populations?
3) It's interesting that the Corsican free-range pigs are at the extreme end of shape divergence (Fig  6a). Not much further is said about this. Not what I would have expected, so what might be the explanation? 4) I'm intrigued by the counter-intuitive (but well-explained in the paper) discussion about reduced mobility and additional increased muscle forces, along with no evidence for size decrease in captivity -but likely an initial increase). Does this perhaps support/explain evidence presented by others using GMM approaches to explore pig domestication, who have claimed the presence of a 'domestic' tooth shape in early Neolithic suids associated with large sized animals indistinguishable in size to wild boar?

07-Feb-2020
Dear Dr Cucchi, It is a pleasure to accept your manuscript entitled "The mark of captivity: plastic responses in the ankle bone of a wild ungulate (Sus scrofa)" in its current form for publication in Royal Society Open Science. The comments of the reviewer(s) who reviewed your manuscript are included at the foot of this letter.
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