The ancestor of all modern domestic cats is the wildcat, Felis silvestris lybica, with archaeological evidence indicating it was domesticated as early as 10,000 years ago in South-West Asia. A recent study, however, claims that cat domestication also occurred in China some 5,000 years ago and involved the same wildcat ancestor (F. silvestris). The application of geometric morphometric analyses to ancient small felid bones from China dating between 5,500 to 4,900 BP, instead reveal these and other remains to be that of the leopard cat (Prionailurus bengalensis). These data clearly indicate that the origins of a human-cat ‘domestic’ relationship in Neolithic China began independently from South-West Asia and involved a different wild felid species altogether. The leopard cat’s ‘domestic’ status, however, appears to have been short-lived—its apparent subsequent replacement shown by the fact that today all domestic cats in China are genetically related to F. silvestris.

Funding: The ERAnet ( https://ec.europa.eu ) Co-Reach project n°137 (European-Chinese Bioarchaeological Collaboration, Euch-Bioarch) led by K. Dobney, and the Chinese Academy of Social Science funded this research. This research was also granted by the Agence National pour la Recherche (ANR, http://www.agence-nationale-recherche.fr/ ), through the LabEx ANR-10-LABX-0003-BCDiv, in the framework of the Investissements d'avenir programme (ANR-11-IDEX-0004-02).

Copyright: © 2016 Vigne et al. This is an open access article distributed under the terms of the Creative Commons Attribution License , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Introduction

With global numbers of more than 500 million individuals, the domestic cat (Felis catus) is amongst the most common pet in the world today. Although modern genetic data indicates that the South-West (SW) Asian and North African subspecies of wildcat (Felis silvestris lybica) is the ancestor of all modern domestic cats [1], both geographic and temporal details regarding its domestication history remain largely conjecture. In Egypt, paintings dating to the 20-19th century BC (Middle Kingdom, 12th Dynasty) have long been considered the earliest clear evidence for cat domestication [2,3]. However, the recent discovery of male and female cat skeletons (along with four kittens belonging to two different litters) at the Egyptian Predynastic elite cemetery of Hierakonpolis (HK6), provides new zooarchaeological evidence for the earlier cultural control of cats during the Naqada IC-IIB period (c. 5800–5600 cal BP—calibrated radiocarbon years before present) [4].

Minor morphological differences observed between the purported wild ancestor (Felis silvestris lybica) and early domestic cats, led scholars to suspect that cat domestication began even earlier than Ancient Egyptian times—at least prior to when visible osteological changes occurred on their skeletons and teeth. Therefore, the presence of cat remains at much earlier archaeological sites from Cyprus (dating from 10,800 to 8,000 cal BP, i.e. Late Pre-Pottery Neolithic A, [PPNA] to Khirokitia phase) [5–8] and another complete cat skeleton tightly associated with a human PPNB burial dating to 9500–9000 cal BP at Shillourokambos [6], provide intriguing evidence for their human introduction to the island and suggest that at least some cats of apparently unchanged wild morphology were not only commensal, but already on their way to being domesticated in SW Asia during the early Holocene.

This early introduction of cats to Cyprus from somewhere in continental SW Anatolia or the Levant may have been a deliberate act on the part of the PPN settlers to deal with a new problem—commensal mice (Mus cypriacus/domesticus). Indeed, the latter began to proliferate with the beginnings of cereal and legume cultivation on the near continent and on Cyprus [7,9–10]. Thus, the origins of our relationship with cats may have been indirectly initiated by the onset of farming in SW Asia, more than 10,800 years ago—a good example of the ‘commensal pathway’ to domestication [6,11–13].

The earliest unquestionable evidence of cats smaller in size than the wildcat (and therefore assumed domestic) dates to the Uruk period (5500–5000 cal BP) from Tell Sheikh Hassan [14]. This evidence suggests that it took several millennia for the domestication process to manifest itself in cats—a likely explanation being the low morphological variability of F. silvestris [15] and/or the extended nature of the commensal relationship with humans.

Recent discoveries have been used to claim cat domestication may also have occurred in Northwest China, following essentially the same commensal pathway as in Egypt and/or SW Asia [16]. Based on the osteometric analyses of eight felid bones found in the Middle-Late Yangshao (Middle Neolithic) agricultural settlement of Quanhucun, Shaanxi Province (directly dated to 5560–5280 cal BP), Hu et al. [16] showed that the Quanhucun cat measurements were smaller than the modern wildcat F. s. lybica and that they also fell within the size range of modern domestic cats. In addition, when collagen stable isotope analysis was undertaken on the same remains, the high δ13C and δ15N values from two of the three Quanhucun cat bones were interpreted as evidence for a diet based on rodents eating the waste of millet farmers (millet is characterized by high δ13C values because of its photosynthesis of C4 plants). In addition, a mandible with surprisingly worn teeth (along with a tibia showing a much lower δ15N value) were taken to indicate that at least some cats from the Quanhucun site “scavenged among or [were] fed by people” (p. 116) and that the commensal status of the Yangshao period cats from Quanhucun could have ultimately resulted in their domestication[16].

On the basis of these data, the authors claimed that the evidence from China provided “the earliest known evidence for a commensal relationship between people and cats” [16] (p. 116), even though the introduction of cats to Cyprus has been shown to be some 4,500 years earlier. Bar-Oz and collaborators have questioned the low δ15N value obtained by Hu et al. for one of the Quanhucun cats, arguing that this value is diagnostic of herbivores and cats are obligate carnivores [17]. They agreed that the Quanhucun cats were likely commensal, but considered that the suggested link between the current evidence and the trajectory of cat domestication in China is tenuous and that, in the absence of a definitive taxonomic identification of the small Quanhucun felid, the data can only be interpreted as evidence of commensalism, not domestication.

Although the past distribution of small felids in Asia remains largely unknown, the relatively small amplitude of the Late Holocene climate change suggests that it should not differ significantly from their modern ranges. Today, four small wild felids live in Shaanxi Province [1,18–22]: the Central Asian wild cat (Felis s. ornata; 1.0–2.1 kg), the Chinese Mountain cat (Felis s. bieti; 4.0–6.5 kg), the Pallas’s cat (Otocolobus manul; 1.8–4.0 kg) and the North Central China subspecies of the leopard cat (Prionailurus b. bengalensis; 1.5–3.8 kg). F. s. bieti can be excluded as a possible match for the published Quanhucun cat because it is much larger and today lives only in mountainous areas. O. manul is phylogenetically intermediate between F. silvestris and P. bengalensis, but its head and mandible are much more massive [23] and, therefore, cannot be confused with the two other species. Consequently, the Quanhucun cats must either derive from local F. s. ornata or P. b. bengalensis (Fig 1a), or alternatively represent early domestic cats (F. s. lybica) imported from SW Asia.

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larger image TIFF original image Download: Fig 1. Modern distribution of wild felid species, archaeological site location and mandible shape relationship between modern wild felid species and domestic cat. (A), Modern Old World distribution of the different wild cat subspecies (Felis silvestris) and the leopard cat (Prionailurus bengalensis), and location of the three Middle-Late Neolithic sites of the Shaanxi and Henan Provinces (China) analyzed in this paper: 1, Quanhucun, 2, Wuzhuangguoliang, 3, Xiawanggang (Redrawn from [http://maps.iucnredlist.org/map.html?id=60354712] and [http://maps.iucnredlist.org/map.html?id=18146] under a CC BY license, with permission from IUCN Red List of Threatened Species; S1 Text.; CAD I. Carrère); (B), Phenotypic relationship (unrooted neighbour joining tree) built on mandible shape distances between modern domestic cat (F. catus), leopard cat (P. bengalensis) and the two relevant sub-species of wild cat (F. s. silvestris; F. s. lybica) from our analyses. https://doi.org/10.1371/journal.pone.0147295.g001

The close phenotypic proximity of these taxa [1, 23–24] prevents their definitive identification by traditional osteometric techniques from isolated and fragmented zooarchaeological remains. We, therefore, applied two dimensional landmark-based geometric approaches to five archaeological Chinese cat mandibles, which included the specimens from Quanhucun studied by Hu et al. [16], and several additional small felids recovered from two Middle and Late Neolithic sites located in Shaanxi and Henan Provinces (Fig 1a, Table 1).

Here we report the results of the comparative study of five archaeological mandibles with modern domestic (F. catus; N = 13) and wild cats: the Northern Chinese sub-species of leopard cat (P. b. bengalensis; N = 10), the European subspecies of wildcat (F. s. silvestris; N = 29) and the SW Asian and North African subspecies of wildcat (F. s. lybica; N = 44) (S1 Table). In order to reaffirm the identification of the Cypriot PPNB cats as F. silvestris [6], we also included five mandibles from the site of Shillourokambos (dated to 9500–9000 cal. BP [27]) in the analyses.