Barbara L. Lundrigan

Ontogeny of integrated skull growth in the cotton rat Sigmodon fulviventer

Because development is epigenetic, diverse aspects of morphology are integrated during ontogeny. Using the method of thin‐plate splines, and the decomposition of these splines by their principal warps, we examine the ontogeny of integrated features of skull growth of the cotton rat, Sigmodon fulviventer as observed in landmark locations in the ventral view. Postnatal growth of the skull in Sigmodon is not adequately described by the familiar contrast between relatively rapid facial elongation and slow, precocial growth of the cranial base. No developmental units corresponding to “facial skull” and “cranial base” emerge from analysis of geometric shape change. Rather, skull growth is both more integrated and more complex, exhibiting both skull‐wide integration and locally individualized regions. Like skull shape, integration has an ontogeny; different regions of the skull can be partitioned into developmentally individualized parts in different ways at different ages. The effective count of individualized parts decreases substantially before weaning occurs, suggesting that the integration required by the functionally demanding activity of chewing gradually develops before the functional transition occurs. Our description of skull growth and integration does not depend upon arbitrary a priori choices about what to measure; rather, we base our decomposition of the whole into parts upon results of the data analysis. Our approach complicates the study of heterochrony, but, because it expresses the spatiotemporal organization of ontogeny, it enables the study of heterotopy.

Phylogenetic Relationships in the Genus Mus, Based on Paternally, Maternally, and Biparentally Inherited Characters

Several species in the rodent genus Mus are used as model research organisms, but comparative studies of these mice have been hampered by the lack of a well-supported phylogeny. We used DNA sequences from six genes representing paternally, maternally, and biparentally inherited regions of the genome to infer phylogenetic relationships among 10 species of Mus commonly used in laboratory research. Our sample included seven species from the subgenus Mus; one species each from the subgenera Pyromys, Coelomys, and Nannomys; and representatives from three additional murine genera, which served as outgroups in the phylogenetic analyses. Although each of the six genes yielded a unique phylogeny, several clades were supported by four or more gene trees. Nodes that conflicted between trees were generally characterized by weak support for one or both of the alternative topologies, thus providing no compelling evidence that any individual gene, or part of the genome, was misleading with respect to the evolutionary history of these mice. Analysis of the combined data resulted in a fully resolved tree that strongly supports monophyly of the genus Mus, monophyly of the subgenus Mus, division of the subgenus Mus into Palearctic (M. musculus, M. macedonicus, M. spicilegus, and M. spretus) and Asian (M. cervicolor, M. cookii, and M. caroli) clades, monophyly of the house mice (M. m. musculus, M. m. molossinus, M. m. castaneus, and M. m. domesticus), and a sister-group relationship between M. macedonicus and M. spicilegus. Other clades that were strongly supported by one or more gene partitions were not strongly supported by the combined data. This appears to reflect a localized homoplasy in one partition obscuring the phylogenetic signal from another, rather than differences in gene or genome histories.

Developmental regulation of skull morphology. I. Ontogenetic dynamics of variance.

SUMMARY Canalization may play a critical role in molding patterns of integration when variability is regulated by the balance between processes that generate and remove variation. Under these conditions, the interaction among those processes may produce a dynamic structure of integration even when the level of variability is constant. To determine whether the constancy of variance in skull shape throughout most of postnatal growth results from a balance between processes generating and removing variation, we compare covariance structures from age to age in two rodent species, cotton rats (Sigmodon fulviventer) and house mice (Mus musculus domesticus). We assess the overall similarity of covariance matrices by the matrix correlation, and compare the structures of covariance matrices using common subspace analysis, a method related to common principal components (PCs) analysis but suited to cases in which variation is so nearly spherical that PCs are ambiguous. We find significant differences from age to age in covariance structure and the more effectively canalized ones tend to be least stable in covariance structure. We find no evidence that canalization gradually and preferentially removes deviations arising early in development as we might expect if canalization results from compensatory differential growth. Our results suggest that (co)variation patterns are continually restructured by processes that equilibrate variance, and thus that canalization plays a critical role in molding patterns of integration.

Social intelligence in the spotted hyena (Crocuta crocuta)

If the large brains and great intelligence characteristic of primates were favoured by selection pressures associated with life in complex societies, then cognitive abilities and nervous systems with primate-like attributes should have evolved convergently in non-primate mammals living in large, elaborate societies in which social dexterity enhances individual fitness. The societies of spotted hyenas are remarkably like those of cercopithecine primates with respect to size, structure and patterns of competition and cooperation. These similarities set an ideal stage for comparative analysis of social intelligence and nervous system organization. As in cercopithecine primates, spotted hyenas use multiple sensory modalities to recognize their kin and other conspecifics as individuals, they recognize third-party kin and rank relationships among their clan mates, and they use this knowledge adaptively during social decision making. However, hyenas appear to rely more intensively than primates on social facilitation and simple rules of thumb in social decision making. No evidence to date suggests that hyenas are capable of true imitation. Finally, it appears that the gross anatomy of the brain in spotted hyenas might resemble that in primates with respect to expansion of frontal cortex, presumed to be involved in the mediation of social behaviour.

Do precocial mammals develop at a faster rate? A comparison of rates of skull development in Sigmodon fulviventer and Mus musculus domesticus

Abstract Variation in neonatal maturity among mammals is often explained by variation in gestation length, but species may also differ in developmental rate, a quantity that is difficult to measure because the conventional formalism makes two important and potentially unrealistic assumptions: (1) ontogeny of form can be described by a single line, and (2) species have the same ontogeny of form. We examine two species, one precocial (Sigmodon fulviventer), the other altricial (Mus musculus domesticus), and find that neither assumption is met. Therefore, we introduce an alternative metric, the rate of shape differentiation away from the average neonate. We find that S. fulviventer has a lower developmental rate than M. m. domesticus; consequently, while more mature at birth, S. fulviventer loses ground to M. m. domesticus over time. Surprisingly, despite differences in gestation length and developmental rate, these species reach developmental and life‐history milestones at nearly identical degrees of skull shape maturity.

Morphology of horns and fighting behavior in the family Bovidae

Horns of bovids are remarkably diverse. This diversity may reflect functional differences associated with the use of horns as intraspecific weapons. I use measurements from museum specimens and behavioral data from the literature to examine the relationship between morphology of horns of males and fighting behavior in 21 species of bovids, representing 11 of the 12 bovid tribes. A high correlation between morphology of horns and fighting behavior was found. In particular, a short horn reach and undeveloped catching arch is associated with stabbing behavior; a long horn reach, with wrestling and fencing behavior; a well-developed catching arch, with wrestling behavior; and robust, recurved horns, with ramming behavior. A phylogeny of bovid tribes suggests that these features of morphology of horns and fighting behavior are rapidly evolving and frequently convergent.

Geographic origin of the Y Chromosomes in "old" inbred strains of mice

Six distinct Y Chromosomes (Chr) were identified among 39 standard inbred strains of mice with five probes that identified Y Chr-specific restriction fragments on Southern blots. Three Y Chr types, distributed among 31 strains, were of Asian Mus musculus origin. The remaining three Y Chr types, distributed among eight strains, were of M. domesticus origin. The Asian source of the M. musculus Y Chr was confirmed by determining the DNA sequence of 221 bp from an open reading frame within the Sry (sex determining region Y) gene (Gubbay et al., Nature 346 245–250, 1990) in three inbred strains (C57BL/6J, AKR/J, and SWR/J) and comparing the sequence to the homologous sequences derived from wild caught European and Asian M. musculus males. These data indicate that a minimum of six male mice contributed to the formation of the old inbred strains.

Mother-young relationships in captive ungulates: variability and clustering

Abstract We recorded four measures of mother-young association and the percentage of time the young spent lying during the first week after birth for 59 mother-young pairs belonging to 22 species and seven families of ungulates. The measures of mother-young association were positively correlated with each other and negatively correlated with the percentage of time the young spent lying. Three cluster analyses, based on various combinations of measures, separated the bovids into two groups recognizable as ‘followers’ and ‘hiders’. When the data on all 22 species were considered, five consistent species groups occurred in the three cluster analyses. The traditional follower-hider dichotomy provides a rough characterization of mother-young relationships in many ungulates, but does not adequately describe the behavioural variation present. By using standardized quantitative measures, we were able to characterize this variation and to establish a framework for future study.

The ontogenetic complexity of developmental constraints

Developmental constraint is a theoretically important construct bridging ontogenetic and evolutionary studies. We propose a new operationalization of this notion that exploits the unusually rich measurement structure of landmark data. We represent landmark configurations by their partial warps, a basis for morphospace that represents a set of localized features of form. A finding of developmental constraint arises from the interplay between age‐varying means and age‐specific variances in these subspaces of morphospace. Examination of variances and means in 16 ventral skull landmarks in the cotton rat S. fulviventer at ages 1, 10, 20, and 30 days yielded three types of developmental constraint: canalization (constraint to relatively constant form age by age); chreods (reduction of variance orthogonal to the mean trajectory over ages); and opposition (reduction of age‐specific variance along the mean trajectory over ages). While canalization and chreodic constraints have been noted previously, the oppositional type of constraint appears novel. Only one of our characters, relative length and orientation of the incisive foramen, appears to be canalized. Although skull growth becomes increasingly integrated through ontogeny, our characters display a remarkable spatiotemporal complexity in patterns of variance reduction. The specific assortment of constraints observed may be related to the precociality of Sigmodon. We suggest that Waddingtons diagrammatic presentation of the “epigenetic landscape” may be misleading in quantitative studies of developmental regulation.

Tests for Positive Selection on Immune and Reproductive Genes in Closely Related Species of the Murine Genus Mus

We examine variation among species of Mus in four genes involved in reproduction and the immune response for evidence of positive selection: the sperm recognition gene Zp-3, the testis-determining locus Sry, the testicular cell surface matrix protein Tcp-1, and the immune system protein β2m. We use likelihood ratio tests in the context of a well-supported phylogeny to determine whether models that allow for positively selected sites fit the sequences better than models that assume purifying selection. We then apply a Bayesian approach to identify particular sites in each gene that have a high posterior probability of being under positive selection. We find no evidence of positive selection on the Tcp-1 gene, but for Zp-3, Sry, and β2m, models that allow for positively selected sites fit the sequences better than alternatives. For each of these genes, we identify sites that have a high (> 95%) posterior probability of being positively selected. For Zp-3, two of these sites occur near the sperm-binding region, while one occurs in a region whose functional role remains unstudied but where the pattern of change predicts functional importance. A single site in Sry shows an elevated rate of replacement substitution but occurs in a region of apparently little functional importance; therefore, relaxation of functional constraints may better explain the rapid evolution of this site. Three sites in β2m have a posterior probability > 50% of being under positive selection. While the functional role for two of these sites is unknown, the third is known to influence the ability of MHC class I molecules to present antigens to the immune system; therefore, the elevated rate of replacement substitutions at this site is consistent with selection acting to promote variability in immune system proteins.