Cranial muscle architecture in wild boar: Does captivity drive ontogenetic trajectories?

The jaw system in mammals is complex and different muscle morphotypes have been documented. Pigs are an interesting group of animals as they are omnivorous and have a bunodont crushing dentition. Moreover, they have interacted with humans for over 10,000 years and grow nearly two orders of magnitude in size. Despite being a model system for studies on cranial form and function, data on the growth of the jaw adductor muscles are scant. Moreover, whether captivity impacts the growth and architecture of the jaw adductors remains unknown. Based on dissection data of the jaw adductors of 45 animals ranging from less than 1 kg to almost 100 kg, we show that muscle masses, muscle fiber lengths, and cross-sectional areas scale as predicted for geometrically similar systems or with slight negative allometry. Only the fiber length of the lateral pterygoid muscle grew with slight positive allometry. Animals raised in captivity in stalls or in an enclosure were overall very similar to wild animals. However, some muscles were larger in captive animals. Interestingly, variation in bite force in captive animals was well predicted by the variation in the size of the superficial masseter muscle relative to the overall jaw adductor mass.

Palaeogenomic analysis of black rat (Rattus rattus) reveals multiple European introductions associated with human economic history.

The distribution of the black rat (Rattus rattus) has been heavily influenced by its association with humans. The dispersal history of this non-native commensal rodent across Europe, however, remains poorly understood, and different introductions may have occurred during the Roman and medieval periods. Here, in order to reconstruct the population history of European black rats, we first generate a de novo genome assembly of the black rat. We then sequence 67 ancient and three modern black rat mitogenomes, and 36 ancient and three modern nuclear genomes from archaeological sites spanning the 1st-17th centuries CE in Europe and North Africa. Analyses of our newly reported sequences, together with published mitochondrial DNA sequences, confirm that black rats were introduced into the Mediterranean and Europe from Southwest Asia. Genomic analyses of the ancient rats reveal a population turnover in temperate Europe between the 6th and 10th centuries CE, coincident with an archaeologically attested decline in the black rat population. The near disappearance and re-emergence of black rats in Europe may have been the result of the breakdown of the Roman Empire, the First Plague Pandemic, and/or post-Roman climatic cooling.

The effect of captivity on craniomandibular and calcaneal ontogenetic trajectories in wild boar.

Deciphering the plastic (i.e., nonheritable) changes induced by human control over wild animals in the archeological record is challenging. Previous studies detected morphological markers associated with captivity in the cranium, mandible, and calcaneus of adult wild boar (Sus scrofa) but the developmental trajectories leading up to these changes during ontogeny remain unknown. To assess the impact of growth in a captive environment on morphological structures during postnatal ontogeny, we used an experimental approach focusing on the same three structures and taxon. We investigated the form and size differences of captive-reared and wild-caught wild boar during growth using three-dimensional landmark-based geometric morphometrics. Our results provide evidence of an influence of captivity on the morphology of craniomandibular structures, as wild specimens are smaller than captive individuals at similar ages. The food resources inherent to anthropogenic environments may explain some of the observed differences between captive-reared and wild specimens. The calcaneus presents a different contrasted pattern of plasticity as captive and wild individuals differ in terms of form but not in terms of size. The physically more constrained nature of the calcaneus and the direct influence of mobility reduction on this bone may explain these discrepancies. These results provide new methodological perspectives for bioarchaeological approaches as they imply that the plastic mark of captivity can be observed in juvenile specimens in the same way it has been previously described in adults.

Bones geometric morphometrics illustrate 10th millennium cal. BP domestication of autochthonous Cypriot wild boar (Sus scrofa circeus nov. ssp).

Epipaleolithic hunter-gatherers from the Near East introduced wild boars (Sus scrofa) to Cyprus, with the Early Pre-Pottery Neolithic (PPN) settlers hunting the wild descendants of these boars. However, the geographic origin of the Cypriot boar and how they were integrated into the earliest forms of pig husbandry remain unsolved. Here, we present data on 11,000 to 9000 cal. BP Sus scrofa from the PPN sites of Klimonas and Shillourokambos. We compared them to contemporaneous populations from the Near East and to Neolithic and modern populations in Corsica, exploring their origin and evolution using biosystematic signals from molar teeth and heel bones (calcanei), using 2D and 3D geometric morphometrics. We found that the Cypriot PPN lineage of Sus scrofa originates from the Northern Levant. Yet, their phenotypic idiosyncrasy suggest that they evolved into an insular sub-species that we named Sus scrofa circeus, referring to Circe, the metamorphosis goddess that changed Ulysses companions into pigs. The phenotypic homogeneity among PPNA Klimonas wild boars and managed populations of PPNB Shillourokambos suggests that local domestication has been undertaken on the endemic S. s. circeus, strengthening the idea that Cyprus was integrated into the core region of animal domestication.

Constraints associated with captivity alter craniomandibular integration in wild boar.

The domestication process is associated with substantial phenotypic changes through time. However, although morphological integration between biological structures is purported to have a major influence on the evolution of new morphologies, little attention has been paid to the influence of domestication on the magnitude of integration. Here, we assessed the influence of constraints associated with captivity, considered as one of the crucial first steps in the domestication process, on the integration of cranial and mandibular structures. We investigated the craniomandibular integration in Western European Sus scrofa using three-dimensional (3D) landmark-based geometric morphometrics. Our results suggest that captivity is associated with a lower level of integration between the cranium and the mandible. Plastic responses to captivity can thus affect the magnitude of integration of key functional structures. These findings underline the critical need to develop integration studies in the context of animal domestication to better understand the processes accountable for the set-up of domestic phenotypes through time.

Investigating the impact of captivity and domestication on limb bone cortical morphology: an experimental approach using a wild boar model.

The lack of bone morphological markers associated with the human control of wild animals has prevented the documentation of incipient animal domestication in archaeology. Here, we assess whether direct environmental changes (i.e. mobility reduction) could immediately affect ontogenetic changes in long bone structure, providing a skeletal marker of early domestication. We relied on a wild boar experimental model, analysing 24 wild-born specimens raised in captivity from 6 months to 2 years old. The shaft cortical thickness of their humerus was measured using a 3D morphometric mapping approach and compared with 23 free-ranging wild boars and 22 pigs from different breeds, taking into account sex, mass and muscle force differences. In wild boars we found that captivity induced an increase in cortical bone volume and muscle force, and a topographic change of cortical thickness associated with muscular expression along a phenotypic trajectory that differed from the divergence induced by selective breeding. These results provide an experimental proof of concept that changes in locomotor behaviour and selective breeding might be inferred from long bones morphology in the fossil and archaeological record. These trends need to be explored in the archaeological record and further studies are required to explore the developmental changes behind these plastic responses.

Tracking the Near Eastern origins and European dispersal of the western house mouse.

The house mouse (Mus musculus) represents the extreme of globalization of invasive mammals. However, the timing and basis of its origin and early phases of dispersal remain poorly documented. To track its synanthropisation and subsequent invasive spread during the develoment of complex human societies, we analyzed 829 Mus specimens from 43 archaeological contexts in Southwestern Asia and Southeastern Europe, between 40,000 and 3,000 cal. BP, combining geometric morphometrics numerical taxonomy, ancient mitochondrial DNA and direct radiocarbon dating. We found that large late hunter-gatherer sedentary settlements in the Levant, c. 14,500 cal. BP, promoted the commensal behaviour of the house mouse, which probably led the commensal pathway to cat domestication. House mouse invasive spread was then fostered through the emergence of agriculture throughout the Near East 12,000 years ago. Stowaway transport of house mice to Cyprus can be inferred as early as 10,800 years ago. However, the house mouse invasion of Europe did not happen until the development of proto urbanism and exchange networks - 6,500 years ago in Eastern Europe and 4000 years ago in Southern Europe - which in turn may have driven the first human mediated dispersal of cats in Europe.

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.

Exploring Rattus praetor (Rodentia, Muridae) as a possible species complex using geometric morphometrics on dental morphology.

Taxonomic uncertainties in the Rattus genus persist due to among-species morphological conservatism coupled with within-species environmental variation in morphology. As a result, this genus contains a number of possible cryptic species. One important example can be found in R. praetor, where morphological studies indicate it is a possible species complex. Genetic studies of R. praetor (limited to analysis of mitochondrial DNA) have been inconclusive, but do indicate such subdivision. Here we use geometric morphometrics to explore this possible species complex by analysing the dental traits of 48 specimens from New Guinea and neighbouring regions. We find separate molar morphologies for Bougainsville Island, central New Guinea and west New Guinea which cannot be easily explained by different environmental factors (climate, precipitation and altitude), strongly suggesting the existence of a number of evolutionarily distinct taxa within what is currently called R. praetor thus supporting previous suggestions that R. praetor is a species complex. Our findings demonstrate the potential of advanced morphological analyses in identifying separate species, contrary to the claims of morphological conservatism. Future analyses should combine geometric morphometrics with genetic analyses over the species range and include sub-fossil specimens from the Bismarck archipelago and Solomon Islands to resolve the evolutionary history of R. praetor.

A test for paedomorphism in domestic pig cranial morphology.

Domestic animals are often described as paedomorphic, meaning that they retain juvenile characteristics into adulthood. Through a three-dimensional landmark-based geometric morphometric analysis of cranial morphology at three growth stages, we demonstrate that wild boar (n = 138) and domestic pigs (n = 106) (Sus scrofa) follow distinct ontogenetic trajectories. With the exception of the size ratio between facial and neurocranial regions, paedomorphism does not appear to be the primary pattern describing the observed differences between wild and domestic pig cranial morphologies. The cranial phenotype of domestic pigs instead involves developmental innovation during domestication. This result questions the long-standing assumption that domestic animal phenotypes are paedomorphic forms of their wild counterparts.

Origins of house mice in ecological niches created by settled hunter-gatherers in the Levant 15,000 y ago.

Reductions in hunter-gatherer mobility during the Late Pleistocene influenced settlement ecologies, altered human relations with animal communities, and played a pivotal role in domestication. The influence of variability in human mobility on selection dynamics and ecological interactions in human settlements has not been extensively explored, however. This study of mice in modern African villages and changing mice molar shapes in a 200,000-y-long sequence from the Levant demonstrates competitive advantages for commensal mice in long-term settlements. Mice from African pastoral households provide a referential model for habitat partitioning among mice taxa in settlements of varying durations. The data reveal the earliest known commensal niche for house mice in long-term forager settlements 15,000 y ago. Competitive dynamics and the presence and abundance of mice continued to fluctuate with human mobility through the terminal Pleistocene. At the Natufian site of Ain Mallaha, house mice displaced less commensal wild mice during periods of heavy occupational pressure but were outcompeted when mobility increased. Changing food webs and ecological dynamics in long-term settlements allowed house mice to establish durable commensal populations that expanded with human societies. This study demonstrates the changing magnitude of cultural niche construction with varying human mobility and the extent of environmental influence before the advent of farming.

Social Complexification and Pig (Sus scrofa) Husbandry in Ancient China: A Combined Geometric Morphometric and Isotopic Approach.

Pigs have played a major role in the economic, social and symbolic systems of China since the Early Neolithic more than 8,000 years ago. However, the interaction between the history of pig domestication and transformations in Chinese society since then, have not been fully explored. In this paper, we investigated the co-evolution from the earliest farming communities through to the new political and economic models of state-like societies, up to the Chinese Empire, using 5,000 years of archaeological records from the Xiawanggang (XWG) and Xinzhai (XZ) sites (Henan Province). To trace the changes of pig populations against husbandry practices, we combined the geometric morphometric analysis of dental traits with a study of the stable carbon and nitrogen isotope ratios from bone collagen. The domestication process intensified during the Neolithic Yangshao, prompted by greater selective pressure and/or better herd control against wild introgression. After that, pig farming, in XWG, relied on local livestock and a gradual change of husbandry practices overtime. This was characterized by a gentle increase in millet foddering and animal protein intake, until a complete change over to household management during the Han dynasty. The only rupture in this steady trend of husbandry occurred during the Longshan period, with the appearance of small sized and idiosyncratic pigs with specific feeding practices (relying on millet and household scraps). From three exploratory hypothesis, we explored the possibility of anti-elite pig production in XWG during the Longshan period, as a means to resist incorporation into a new economic model promoting intensified domestic production. This exploratory hypothesis is the most suitable to our dataset; however, numerous areas need to be explored further in order to adequately document the role of pigs in the rise of China's complex societies.

An Ecological and Evolutionary Framework for Commensalism in Anthropogenic Environments.

Commensalism within anthropogenic environments has not been extensively discussed, despite its impact on humans, and there is no formal framework for assessing this ecological relationship in its varied forms. Here, we examine commensalism in anthropogenic environments in detail, considering both ecological and evolutionary drivers. The many assumptions about commensalism and the nature of anthropogenic environments are discussed and we highlight dependency as a key attribute of anthropogenic commensals (anthrodependent taxa). We primarily focus on mammalian species in the anthropogenic-commensal niche, but the traits described and selective pressures presented are likely fundamental to many species engaged in intense commensal relationships with humans. Furthermore, we demonstrate that this largely understudied interaction represents an important opportunity to investigate evolutionary processes in rapidly changing environments.

Earliest "Domestic" Cats in China Identified as Leopard Cat (Prionailurus bengalensis).

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.

Phenotype and animal domestication: A study of dental variation between domestic, wild, captive, hybrid and insular Sus scrofa.

BACKGROUND: Identifying the phenotypic responses to domestication remains a long-standing and important question for researchers studying its early history. The great diversity in domestic animals and plants that exists today bears testament to the profound changes that domestication has induced in their ancestral wild forms over the last millennia. Domestication is a complex evolutionary process in which wild organisms are moved to new anthropogenic environments. Although modern genetics are significantly improving our understanding of domestication and breed formation, little is still known about the associated morphological changes linked to the process itself. In order to explore phenotypic variation induced by different levels of human control, we analysed the diversity of dental size, shape and allometry in modern free-living and captive wild, wild x domestic hybrid, domestic and insular Sus scrofa populations. RESULTS: We show that domestication has created completely new dental phenotypes not found in wild boar (although the amount of variation amongst domestic pigs does not exceed that found in the wild). Wild boar tooth shape also appears to be biogeographically structured, likely the result of post-glacial recolonisation history. Furthermore, distinct dental phenotypes were also observed among domestic breeds, probably the result of differing types and intensity of past and present husbandry practices. Captivity also appears to impact tooth shape. Wild x domestic hybrids possess second molars that are strictly intermediate in shape between wild boar and domestic pigs (third molars, however, showing greater shape similarity with wild boar) while their size is more similar to domestic pigs. The dental phenotypes of insular Sus scrofa populations found on Corsica and Sardinia today (originally introduced by Neolithic settlers to the islands) can be explained either by feralization of the original introduced domestic swine or that the founding population maintained a wild boar phenotype through time. CONCLUSIONS: Domestication has driven significant phenotypic diversification in Sus scrofa. Captivity (environmental control), hybridization (genome admixture), and introduction to islands all correspond to differing levels of human control and may be considered different stages of the domestication process. The relatively well-known genetic evolutionary history of pigs shows a similar complexity at the phenotypic level.

Unravelling the complexity of domestication: a case study using morphometrics and ancient DNA analyses of archaeological pigs from Romania.

Current evidence suggests that pigs were first domesticated in Eastern Anatolia during the ninth millennium cal BC before dispersing into Europe with Early Neolithic farmers from the beginning of the seventh millennium. Recent ancient DNA (aDNA) research also indicates the incorporation of European wild boar into domestic stock during the Neolithization process. In order to establish the timing of the arrival of domestic pigs into Europe, and to test hypotheses regarding the role European wild boar played in the domestication process, we combined a geometric morphometric analysis (allowing us to combine tooth size and shape) of 449 Romanian ancient teeth with aDNA analysis. Our results firstly substantiate claims that the first domestic pigs in Romania possessed the same mtDNA signatures found in Neolithic pigs in west and central Anatolia. Second, we identified a significant proportion of individuals with large molars whose tooth shape matched that of archaeological (likely) domestic pigs. These large 'domestic shape' specimens were present from the outset of the Romanian Neolithic (6100-5500 cal BC) through to later prehistory, suggesting a long history of admixture between introduced domestic pigs and local wild boar. Finally, we confirmed a turnover in mitochondrial lineages found in domestic pigs, possibly coincident with human migration into Anatolia and the Levant that occurred in later prehistory.