Madeleine Geiger

The taming of the neural crest: a developmental perspective on the origins of morphological covariation in domesticated mammals

Studies on domestication are blooming, but the developmental bases for the generation of domestication traits and breed diversity remain largely unexplored. Some phenotypic patterns of human neurocristopathies are suggestive of those reported for domesticated mammals and disrupting neural crest developmental programmes have been argued to be the source of traits deemed the ‘domestication syndrome’. These character changes span multiple organ systems and morphological structures. But an in-depth examination within the phylogenetic framework of mammals including domesticated forms reveals that the distribution of such traits is not universal, with canids being the only group showing a large set of predicted features. Modularity of traits tied to phylogeny characterizes domesticated mammals: through selective breeding, individual behavioural and morphological traits can be reordered, truncated, augmented or deleted. Similarly, mammalian evolution on islands has resulted in suites of phenotypic changes like those of some domesticated forms. Many domesticated mammals can serve as valuable models for conducting comparative studies on the evolutionary developmental biology of the neural crest, given that series of their embryos are readily available and that their phylogenetic histories and genomes are well characterized.

Cranial Suture Closure in Domestic Dog Breeds and Its Relationships to Skull Morphology.

Bulldog‐type brachycephalic domestic dog breeds are characterized by a relatively short and broad skull with a dorsally rotated rostrum (airorhynchy). Not much is known about the association between a bulldog‐type skull conformation and peculiar patterns of suture and synchondrosis closure in domestic dogs. In this study, we aim to explore breed‐specific patterns of cranial suture and synchondrosis closure in relation to the prebasial angle (proxy for airorhynchy and thus bulldog‐type skull conformation) in domestic dogs. For this purpose, we coded closure of 18 sutures and synchondroses in 26 wolves, that is, the wild ancestor of all domestic dogs, and 134 domestic dogs comprising 11 breeds. Comparisons of the relative amount of closing and closed sutures and synchondroses (closure scores) in adult individuals showed that bulldog‐type breeds have significantly higher closure scores than non‐bulldog‐type breeds and that domestic dogs have significantly higher closure scores than the wolf. We further found that the prebasial angle is significantly positively correlated with the amount of closure of the basispheno‐presphenoid synchondrosis and sutures of the nose (premaxillo‐nasal and maxillo‐nasal) and the palate (premaxillo‐maxillary and interpalatine). Our results show that there is a correlation between patterns of suture and synchondrosis closure and skull shape in domestic dogs, although the causal relationships remain elusive. Anat Rec, 299:412–420, 2016.

Neomorphosis and heterochrony of skull shape in dog domestication

The overall similarity of the skull shape of some dog breeds with that of juvenile wolves begs the question if and how ontogenetic changes such as paedomorphosis (evolutionary juvenilisation) played a role in domestication. Here we test for changes in patterns of development and growth during dog domestication. We present the first geometric morphometric study using ontogenetic series of dog and wolf crania, and samples of dogs with relatively ancestral morphology and from different time periods. We show that patterns of juvenile-to-adult morphological change are largely similar in wolves and domestic dogs, but differ in two ways. First, dog skulls show unique (neomorphic) features already shortly after birth, and these features persist throughout postnatal ontogeny. Second, at any given age, juvenile dogs exhibit skull shapes that resemble those of consistently younger wolves, even in dog breeds that do not exhibit a ‘juvenilized’ morphology as adults. These patterns exemplify the complex nature of evolutionary changes during dog domestication: the cranial morphology of adult dogs cannot simply be explained as either neomorphic or paedomorphic. The key to our understanding of dog domestication may lie in a closer comparative examination of developmental phases.

Unaltered sequence of dental, skeletal, and sexual maturity in domestic dogs compared to the wolf.

BackgroundIt has been hypothesised that domestication altered the sequence of dental, skeletal, and sexual maturity of dogs when compared to their wolf ancestor. To test this we investigated a comprehensive sample of domestic dogs.MethodsWe documented the timing of completed eruption of permanent dentition into occlusion (dental maturity) and the timing of growth plate closure at the proximal humerus (skeletal maturity) in ontogenetic series of wolves and 15 domestic dog breeds. Data for 137 domestic dog and 64 wolf individuals were collected based on radiographs and examination of macerated bones.ResultsOur analyses show that domestic dogs exhibit a similar sequence of dental and skeletal maturity as the ancestral wolf. Although the absolute change of the age at attainment of sexual maturity is great in domestic dogs as compared to the wolf, the sequence of dental, skeletal, and sexual maturity is not altered as extensively, contradicting one previous hypothesis. Moreover, our data suggest that the chondrodystrophic dachshund attains skeletal maturity earlier than the non-chondrodystrophic breeds examined here.ConclusionsDomestic dogs are more wolf-like in terms of the sequence of dental, skeletal, and sexual maturation than previously hypothesised. This implies that the domestication process and/or breed formation did not have a major impact on this sequence, although the absolute values of life history variables do have a greater range of variation than in the wild wolf.

Ontogeny of domestic dogs and the developmental foundations of carnivoran domestication

Whereas hundreds of breeds of domestic dogs are known, only several dozen domestic cat breeds are currently recognized, and the ferret is not classified into specific breeds. We studied pre- and postnatal patterns of development and growth in the domesticated forms of these three carnivoran species. We present the most comprehensive staging system for domestic dog embryos to date and define qualitative characters for phylogenetic comparisons. For postnatal development, we present analyses of new and literature measurements of cranial and limb proportions. We analyze changes in the progress of growth among different domestic dog and domestic cat breeds. All three domesticated forms drastically differ in the relative timing of prenatal development. This is correlated with ontogenetic plasticity at birth, which enables artificial selection to act. For postnatal development, we detected a greater shape variance in domestic dog ontogeny when compared to that of the domestic cat. We conclude that ontogenetic preconditions as well as body size constrain the species’ capability for artificial selection in domestic dogs and cats. However, we speculate that the human requirements for functional performance of their domesticates might render some developmental biases substantially. Although ferrets would be preferable for artificial selection given their plastic embryonic development, they have been of less interest for domestication due to their small body size - by which they were already well adapted for hunting in burrows - and due to the fact that other relevant tasks were already assumed by domestic cats and dogs since earlier phases of human cultural evolution.

Growth trajectories in the cave bear and its extant relatives: an examination of ontogenetic patterns in phylogeny

BackgroundThe study of postnatal ontogeny can provide insights into evolution by offering an understanding of how growth trajectories have evolved resulting in adult morphological disparity. The Ursus lineage is a good subject for studying cranial and mandibular shape and size variation in relation to postnatal ontogeny and phylogeny because it is at the same time not diverse but the species exhibit different feeding ecologies. Cranial and mandibular shapes of Ursus arctos (brown bear), U. maritimus (polar bear), U. americanus (American black bear), and the extinct U. spelaeus (cave bear) were examined, using a three-dimensional geometric morphometric approach. Additionally, ontogenetic series of crania and mandibles of U. arctos and U. spelaeus ranging from newborns to senile age were sampled.ResultsThe distribution of specimens in morphospace allowed to distinguish species and age classes and the ontogenetic trajectories U. arctos and U. spelaeus were found to be more similar than expected by chance. Cranial shape changes during ontogeny are largely size related whereas the evolution of cranial shape disparity in this clade appears to be more influenced by dietary adaptation than by size and phylogeny. The different feeding ecologies are reflected in different cranial and mandibular shapes among species.ConclusionsThe cranial and mandibular shape disparity in the Ursus lineage appears to be more influenced by adaptation to diet than by size or phylogeny. In contrast, the cranial and mandibular shape changes during postnatal ontogeny in U. arctos and U. spelaeus are probably largely size related. The patterns of morphospace occupation of the cranium and the mandible in adults and through ontogeny are different.

On the lack of a universal pattern associated with mammalian domestication: differences in skull growth trajectories across phylogeny

As shown in a taxonomically broad study, domestication modifies postnatal growth. Skull shape across 1128 individuals was characterized by 14 linear measurements, comparing 13 pairs of wild versus domesticated forms. Among wild forms, the boar, the rabbit and the wolf have the highest proportion of allometric growth, explaining in part the great morphological diversity of the domesticated forms of these species. Wild forms exhibit more isometric growth than their domesticated counterparts. Multivariate comparisons show that dogs and llamas exhibit the greatest amount of differences in trajectories with their wild counterparts. The least amount is recorded in the pig–boar, and camel and horse pairs. Bivariate analyses reveal that most domesticated forms have growth trajectories different from their respective wild counterparts with regard to the slopes. In pigs and camels slopes are shared and intercepts are different. There is a trajectory extension in most domesticated herbivores and the contrary pattern in carnivorous forms. However, there is no single, universal and global pattern of paedomorphosis or any other kind of heterochrony behind the morphological diversification that accompanies domestication.

Geographic variation in responses of European yellow dung flies to thermal stress

Climatic conditions can be very heterogeneous even over small geographic scales, and are believed to be major determinants of the abundance and distribution of species and populations. Organisms are expected to evolve in response to the frequency and magnitude of local thermal extremes, resulting in local adaptation. Using replicate yellow dung fly (Scathophaga stercoraria; Diptera: Scathophagidae) populations from cold (northern Europe) and warm climates (southern Europe), we compared 1) responses to short-term heat and cold shocks in both sexes, 2) heat shock protein (Hsp70) expression in adults and eggs, and 3) female reproductive traits when facing short-term heat stress during egg maturation. Contrary to expectations, thermal traits showed minor geographic differentiation, with weak evidence for greater heat resistance of southern flies but no differentiation in cold resistance. Hsp70 protein expression was little affected by heat stress, indicating systemic rather than induced regulation of the heat stress response, possibly related to this fly groups preference for cold climes. In contrast, sex differences were pronounced: males (which are larger) endured hot temperatures longer, while females featured higher Hsp70 expression. Heat stress negatively affected various female reproductive traits, reducing first clutch size, overall reproductive investment, egg lipid content, and subsequent larval hatching. These responses varied little across latitude but somewhat among populations in terms of egg size, protein content, and larval hatching success. Several reproductive parameters, but not Hsp70 expression, exhibited heritable variation among full-sib families. Rather than large-scale clinal geographic variation, our study suggests some local geographic population differentiation in the ability of yellow dung flies to buffer the impact of heat stress on reproductive performance.