Analysis of Polycerate Mutants Reveals the Evolutionary Co-option of HOXD1 for Horn Patterning in Bovidae.

In the course of evolution, pecorans (i.e., higher ruminants) developed a remarkable diversity of osseous cranial appendages, collectively referred to as "headgear," which likely share the same origin and genetic basis. However, the nature and function of the genetic determinants underlying their number and position remain elusive. Jacob and other rare populations of sheep and goats are characterized by polyceraty, the presence of more than two horns. Here, we characterize distinct POLYCERATE alleles in each species, both associated with defective HOXD1 function. We show that haploinsufficiency at this locus results in the splitting of horn bud primordia, likely following the abnormal extension of an initial morphogenetic field. These results highlight the key role played by this gene in headgear patterning and illustrate the evolutionary co-option of a gene involved in the early development of bilateria to properly fix the position and number of these distinctive organs of Bovidae.

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.

Genetic analysis of new progesterone-based fertility traits in dairy cows measured on-farm.

The objectives of this study were (1) to analyze the agreement of a standard laboratory ELISA for progesterone (P4) with an automated on-farm ELISA kit operated under commercial conditions in 1,297 milk samples from 50 dairy cows; (2) to study the influence of the method of detection of luteal activity on genetic parameters of fertility traits based on P4 measured with an automated on-farm ELISA once weekly from wk 3 to 9 postpartum in the milk of 1,304 cows; and (3) to study the influence of sampling frequency (once or twice weekly from wk 3 to 9) on the same traits from 296 cows. Luteal activity can be detected when there is an active corpus luteum in the ovary producing P4 and indicating the onset of reproductive cyclicity after calving. The on-farm ELISA overestimated P4 contents by a mean square error of prediction of 2.76 ng/mL and had an intermediate Spearman correlation with the laboratory kit (0.54). For the second objective, the postpartum interval to the commencement of luteal activity (C-LA), proportion of luteal activity between d 15 and 63 postpartum (P-LA), calculated as the number of samples above the threshold for high P4 values divided by the number of all samples, and delay of first ovulation (DOV1), defined as C-LA occurring later than d 45 postpartum, were derived from the P4 profiles. Both C-LA and DOV1 were determined by (a) thorough qualitative visual inspection of the profile, (b) the profile's mean as threshold for the first increase in P4 postpartum, indicating commencement of luteal activity, and (c) 3 ng/mL as threshold for the first increase in P4, a value that has been used by many other studies. Similarly, P-LA was determined by using methods (b) and (c). Estimates of heritability were 0.04 to 0.13 for C-LA, 0.12 to 0.23 for P-LA, and 0.03 to 0.07 for DOV1. Genetic correlation of P-LA with C-LA and with the profile's mean P4 was -1.00. The profile's mean had a higher estimate of heritability (0.11-0.12) than C-LA or DOV1. It can be calculated as the arithmetic mean of all P4 values of a profile, whereas C-LA, P-LA, and DOV1 need a definition of a threshold for high P4 values. We therefore suggest the profile's mean as a promising candidate for further research. For the third objective, once-weekly sampling was mimicked by neglecting every second sample, and C-LA and DOV1 shifted toward a later onset of cyclicity. Thus, a common standard for sampling regimen and detection algorithm is essential to avoid incompatibility between studies.

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.

ZooMS confirms geometric morphometrics species identification of ancient sheep and goat.

Geometric morphometrics can effectively distinguish isolated third lower molars of present-day sheep and goat, but its applicability to archaeological specimens has yet to be established. Using a modern reference collection of 743 sheep and goats and a two-dimensional landmark-based geometric morphometric (GMM) protocol, this study aimed to morphometrically identify 109 archaeological specimens, used as case studies, dating from the Late Neolithic to the modern period/era. These morphometric identifications were then compared to molecular identifications via collagen peptide mass fingerprinting, known as Zooarcheology by Mass Spectrometry (ZooMS). ZooMS confirmed the morphometric identifications for 104 specimens, with the five misidentified specimens all morphometrically identified as goat. Modern sheep and goats have larger teeth and distinct shapes compared to their archaeological counterparts, suggesting strong differences between archaeological and modern specimens potentially linked with recent breed improvement or geographical origin of the specimens. In addition, for both species, some of the archaeological dental morphologies do not match with any of our modern references. This study validates the applicability of geometric morphometrics for identifying isolated archaeological sheep and goat teeth. It represents a stepping stone for future, non-destructive, bioarchaeological studies of the two species.

Cranial shape diversification in horses: variation and covariation patterns under the impact of artificial selection.

The potential of artificial selection to dramatically impact phenotypic diversity is well known. Large-scale morphological changes in domestic species, emerging over short timescales, offer an accelerated perspective on evolutionary processes. The domestic horse (Equus caballus) provides a striking example of rapid evolution, with major changes in morphology and size likely stemming from artificial selection. However, the microevolutionary mechanisms allowing to generate this variation in a short time interval remain little known. Here, we use 3D geometric morphometrics to quantify skull morphological diversity in the horse, and investigate modularity and integration patterns to understand how morphological associations contribute to cranial evolvability in this taxon. We find that changes in the magnitude of cranial integration contribute to the diversification of the skull morphology in horse breeds. Our results demonstrate that a conserved pattern of modularity does not constrain large-scale morphological variations in horses and that artificial selection has impacted mechanisms underlying phenotypic diversity to facilitate rapid shape changes. More broadly, this study demonstrates that studying microevolutionary processes in domestic species produces important insights into extant phenotypic diversity.

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.

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.

Evolutionary Genomics and Conservation of the Endangered Przewalski's Horse.

Przewalski's horses (PHs, Equus ferus ssp. przewalskii) were discovered in the Asian steppes in the 1870s and represent the last remaining true wild horses. PHs became extinct in the wild in the 1960s but survived in captivity, thanks to major conservation efforts. The current population is still endangered, with just 2,109 individuals, one-quarter of which are in Chinese and Mongolian reintroduction reserves [1]. These horses descend from a founding population of 12 wild-caught PHs and possibly up to four domesticated individuals [2-4]. With a stocky build, an erect mane, and stripped and short legs, they are phenotypically and behaviorally distinct from domesticated horses (DHs, Equus caballus). Here, we sequenced the complete genomes of 11 PHs, representing all founding lineages, and five historical specimens dated to 1878-1929 CE, including the Holotype. These were compared to the hitherto-most-extensive genome dataset characterized for horses, comprising 21 new genomes. We found that loci showing the most genetic differentiation with DHs were enriched in genes involved in metabolism, cardiac disorders, muscle contraction, reproduction, behavior, and signaling pathways. We also show that DH and PH populations split ∼45,000 years ago and have remained connected by gene-flow thereafter. Finally, we monitor the genomic impact of ∼110 years of captivity, revealing reduced heterozygosity, increased inbreeding, and variable introgression of domestic alleles, ranging from non-detectable to as much as 31.1%. This, together with the identification of ancestry informative markers and corrections to the International Studbook, establishes a framework for evaluating the persistence of genetic variation in future reintroduced populations.