Precocial Mammals Research Articles

Modeling Transformations of Neurodevelopmental Sequences across Mammalian Species

A general model of neural development is derived to fit 18 mammalian species, including humans, macaques, several rodent species, and six metatherian (marsupial) mammals. The goal of this work is to describe heterochronic changes in brain evolution within its basic developmental allometry, and provide an empirical basis to recognize equivalent maturational states across animals. The empirical data generating the model comprises 271 developmental events, including measures of initial neurogenesis, axon extension, establishment, and refinement of connectivity, as well as later events such as myelin formation, growth of brain volume, and early behavioral milestones, to the third year of human postnatal life. The progress of neural events across species is sufficiently predictable that a single model can be used to predict the timing of all events in all species, with a correlation of modeled values to empirical data of 0.9929. Each species' rate of progress through the event scale, described by a regression equation predicting duration of development in days, is highly correlated with adult brain size. Neural heterochrony can be seen in selective delay of retinogenesis in the cat, associated with greater numbers of rods in its retina, and delay of corticogenesis in all species but rodents and the rabbit, associated with relatively larger cortices in species with delay. Unexpectedly, precocial mammals (those unusually mature at birth) delay the onset of first neurogenesis but then progress rapidly through remaining developmental events.

Maturation of the growth axis in marsupials occurs gradually during post-natal life and over an equivalent developmental stage relative to eutherian species

The separation of a nutrition-responsive insulin-like growth factor (IGF) system and a growth hormone (GH) responsive IGF system to control pre- and post-natal growth of developing mammals may originate from the constraints imposed by intra-uterine development. In eutherian species that deliver relatively precocial young, maturation of the GH regulatory system is coincident with the time of birth. We measured the hepatic expression of the four key growth axis genes GH-receptor, IGF-1 and -2, and IGFBBP-3, and plasma protein concentrations of IGF-1 from late fetal life through to adult stages of a marsupial, the tammar wallaby. The data clearly show that maturation of GH-regulated growth in marsupials occurs gradually over the course of post-natal life at an equivalent developmental stage to that of precocial eutherian mammals. This suggests that the timing of GH-regulated growth in marsupials is not related to parturition but instead to the relative developmental stage.

Ontogeny of long bone geometry in capuchin monkeys (Cebus albifrons and Cebus apella): implications for locomotor development and life history.

Studies of a diverse array of animals have found that young individuals often have robust bones for their body size (i.e. augmented cross-sectional dimensions), limiting fracture risk despite general musculoskeletal immaturity. However, previous research has focused primarily on precocial taxa (e.g. rodents, lagomorphs, bovids, goats and emu). In this study, we examined the ontogenetic scaling of humeral and femoral cross-sectional robusticity in a mixed-longitudinal sample of two slow-growing, behaviourally altricial capuchin monkeys. Results showed that, when regressed against biomechanically appropriate size variables (i.e. the product of body mass and bone length), humeral and femoral bending strengths generally scale with negative allometry, matching the scaling patterns observed in previous studies of more precocial mammals. Additionally, bone strength relative to predicted loads (e.g. 'safety factors') peaks at birth and rapidly decreases during postnatal growth, falling to less than 5 per cent of peak values by weaning age. We suggest that increased safety factors during early ontogeny may be an adaptation to mitigate injury from falling during initial locomotor efforts. Overall, the results presented here suggest that ontogenetic declines in relative long bone strength may represent a common pattern among mammals that is perhaps preadaptive for different purposes among different lineages.

Age at maturity in cavies: Are precocial mammals different?

In short-lived mammals, age at maturity is a particularly important parameter influencing lifetime fitness. Age at maturity proves highly variable in altricial rodents, but little is known for small precocial rodents of the order Caviomorpha. Even though extreme precociality implies early maturation, female cavies and guinea-pigs (genus Cavia) advance puberty considerably in the presence of males. We briefly review earlier findings and compare them to data from altricial rodents. We report experiments on 2 very similar species of cavy, the dark-backed (C. magna) and the wild cavy (C. aperea). In the dark-backed cavy, we tested whether the male signal responsible for acceleration of maturity is a chemical in urine, as demonstrated for mice. Females exposed twice daily to male urine on their nares matured at the same age (73–75 d) and mass (around 330 g, 4 times birth mass) as females treated with water. Thus, chemicals in urine did not replace the effect of male presence. Two experiments with wild cavies showed that male presence without physical contact was sufficient to accelerate puberty, even though physical interaction leads to even earlier maturation. Presence of a male during the first 10 d of life only did not lead to advanced maturation in young females. Functionally, it may be more correct to speak of a delay in the onset of maturity in the absence of males rather than considering male presence to stimulate early maturation. Comparative evidence suggests that precocial species generally mature earlier than altricials.

Vocal mother–pup communication in guinea pigs: effects of call familiarity and female reproductive state

Vocal communication is of special importance in mother-offspring interactions in many precocial mammals, where the offspring are highly mobile. Newborn guinea pigs, Cavia aperea f. porcellus, make distinct calls when separated from their mother. Assuming that offspring separation calls are important in mother-offspring communication, we predicted guinea pig females would respond more strongly to calls of their own than to calls from unfamiliar pups or other guinea pig calls and would respond to pup calls only during lactation when responses are adaptive. In playback experiments, we tested lactating females' responses to separation calls from their own pups and from unfamiliar pups and to female contact calls. We also tested responses by females in late pregnancy (days 50-60) to separation pup calls. Lactating females responded with significantly more vocalizations to their own and to unfamiliar pup calls than to control sounds. Mothers also responded significantly more strongly to playback of calls from their own pups than to calls from unfamiliar pups, suggesting that mothers are able to use vocal cues in pup recognition. The reproductive state significantly influenced responses: lactating females always responded to pup calls, whereas pregnant females did not respond, suggesting that responsiveness is state dependent.

Perinatal size and maturation of the olfactory and vomeronasal neuroepithelia in lorisoids and lemuroids

Explanations for the chemosensory abilities of newborn mammals focus primarily on food (milk) acquisition and communication (e.g., maternal-infant bonding). However, the relative importance of the main and accessory (vomeronasal) olfactory systems is hypothesized to differ at birth between altricial and precocial mammals. Strepsirrhines (lemurs and lorises) possess main and accessory olfactory systems, and vary in life-history traits related to infant dependency and maturation. Accordingly, this study examines the size and maturational characteristics of vomeronasal (VNNE) and olfactory (OE) neuroepithelia in strepsirrhines. Serially sectioned heads of 18 infant cadavers were examined microscopically for neuroepithelial distribution. Measurements were taken on the length of the nasal fossa on one side that was occupied by VNNE and OE. The data were corrected for body size using the cranial length or body mass, and were then examined for correlation with several life-history variables, as well as activity pattern. In addition, immunohistochemistry was used to identify cells in the VNNE and OE that express olfactory marker protein (OMP), a marker of mature olfactory neurons. Relative OE extent was not significantly correlated with any of the life-history variables. Relative VNNE length was negatively correlated with relative gestation length and relative neonatal mass (P<0.05). However, when we corrected for phylogenetic relationships, we found no significant correlations between either of the neuroepithelial measurements and life-history variables. Immunohistochemical findings suggest that OE has more OMP-reactive cells than VNNE in all species. OMP-reactive cells appear to be less numerous in diurnal species compared to most nocturnal species. These results indicate that the VNNE may be relatively longer at birth in altricial species. However, it remains uncertain how phylogeny and/or ontogeny may explain these findings.

Postural development in rats

Mammals adopt a limited number of postures during their day-to-day activities. These stereotyped skeletal configurations are functionally adequate and limit the number of degrees of freedom to be controlled by the central nervous system. The temporal pattern of emergence of these configurations in altricial mammals is unknown. We therefore carried out an X-ray study in unrestrained rats from birth (P0) until postnatal day 23 (P23). The X-rays showed that many of the skeletal configurations described in adult rodents were already present at birth. By contrast, limb placement changed abruptly at around P10. These skeletal configurations, observed in anesthetized pups, required the maintenance of precise motor control. On the other hand, motor control continued to mature, as shown by progressive changes in resting posture and head movements from P0 to P23. We suggest that a few innate skeletal configurations provide the necessary frames of reference for the gradual construction of an adult motor repertoire in altricial mammals, such as the rat. The apparent absence of a requirement for external sensorial cues in the maturation of this repertoire may account for the maturation of postural and motor control in utero in precocial mammals (Muir et al., 2000 for a review on the locomotor behavior of altricial and precocial animals).

The cost of a specific immune response in young guinea pigs

The specific immune system is a protective mechanism that detects infection and fights it by production of antibodies. Newborns are especially susceptible to infections because their immune system is not yet as fully developed as that of adults. This has been well established in altricial mammals. Fighting infection is associated with costs (metabolic rate, protein synthesis) potentially affecting other developmental processes. We investigated the specific immune response in a precocial mammal, by testing the response of 3 and 7 day old young guinea pigs ( Cavia aperea f. porcellus) against a non-pathogenic antigen (KLH) and determined the effect of the immune response on growth and metabolic rate. Challenged young produced a substantial specific immune response (IgG). The efficiency of the immune response was almost identical in 3 and 7 day old young, but lower than in adult females. Antibody titres achieved by actively immunised young pups were as high as titres transferred transplacentally by mothers immunised on day 40 and 47 of pregnancy. In comparison to a control group, the immune response did not influence growth and metabolic rate measured on day 4 after each immune challenge and was not reflected by changes in hematocrit value. We discuss whether the weaker immune response of pups is caused by reduced allocation of limited resources in growing young or by the immature immune system of young animals.

Maternal food restriction delays weaning in the guinea pig, Cavia porcellus

In mammals, the duration of lactation varies much more than other life history parameters in relation to body mass, both within and between species. The causes of this variation are poorly understood and seem to result from varying conditions of mothers and young. We studied the effect of long-term maternal food restriction on litter mass at birth, duration of lactation and offspring development in the precocial guinea pig. Mild experimental food restriction during reproduction resulted in prolonged nursing behaviour of mothers. Evidence for a threshold mass at weaning was, however, equivocal. In the guinea pig, benefits of prolonged lactation prove hard to understand, because nutritional benefits are minor. Independently of maternal food regime, pups terminated suckling attempts several days after mothers ceased nursing behaviour. The time between the last nursing behaviour and the last suckling attempts was not longer in litters with higher need, that is, in litters of food-restricted females, than in litters of females fed ad libitum. Under food restriction, mothers maintained their own body mass, leading in pups to lower mass at birth, reduced postnatal growth and lower body mass at maturity. Guinea pig mothers appear to be selected to value their own condition more than that of a litter. We suggest that lengthening of the nursing period under poor conditions is a life history response primarily of precocial mammals.

Variation in growth form and precocity at birth in eutherian mammals.

Using the flexible Chapman-Richards model for describing the growth curves from birth to adulthood of 69 species of eutherian mammals, we demonstrate that growth form differs among eutherian mammals. Thereby the commonly used Gompertz model can no longer be considered as the general model for describing mammalian growth. Precocial mammals have their peak growth rate earlier in the growth process than altricial mammals. However, the position on the altricial-precocial continuum accounts for most growth-form differences only between mammalian lineages. Within mammalian genera differences in growth form are not related to precocity at birth. This indicates that growth form may have been associated with precocity at birth early in mammalian evolution, when broad patterns of body development radiated. We discuss four non-exclusive interpretations to account for the role of precocity at birth on the observed variation in growth form among mammals. Precocial and altricial mammals could differ according to (i) the distribution of energy output by the mother, (ii) the ability of the young to assimilate the milk yield, (iii) the allocation of energy by the young between competing functions and (iv) the position of birth between conception and attainment of physical maturity.

Staging and Ageing of Mammalian Embryos and Fetuses

S tiS r b a 0.: Staging and Ageing of Mammalian Embryos and Fetuses. Acta vet. Hmo, 1995,64: 83-89. The objective of this study was to elaborate a method of estimating the age of embryos and fetuses of mammals of unknown ontogenetic age, applicable to both altricial and precocial mammals showing different duration of intrauterine development. The method consists of two steps: First, the embryo or fetus under study has to be staged. It is measured, weighed and classified according to the characteristics given below, in one of the 13 comparable ontogenetic stages. The second step is ageing: the staged embryo is placed in a point on the regression curve of the respective developmental stage that corresponds to the·duration of intrauterine development. The characteristics of the comparable developmental stages, the regression curves and the way in which they are calculated are presented. This method makes it possible to estimate the age of mammalian embryos and fetuses of unknown ontogenetic age, even of those already sectioned in histological series. In this way it is also possible to estimate the rates of morphogenetic events, the growth rate of the whole embryo or of its individual parts and/or organs. Ageing, embryos, fetuses, comparable developmental stages, mammals, staging, regression age curves

Peripheral Deiodination of Thyroid Hormones: Biological Significance

The main secretory product of the thyroid gland is thyroxine (T4), which is a relatively inactive prohormone serving as a substrate for deiodination processes in peripheral tissues. Activation and inactivation of 3,5,3'-triiodo-L-thyronine (T3) occurs in the presence of outer-ring (ORD) and inner-ring deiodinases (IRD), respectively. During ontogenesis high plasma levels of T3 occur at parturition or hatching in precocial mammals and birds and at metamorphic climax in amphibians. These high levels may be obtained by increased T4 ORD activity and also by decreased T3 IRD activity resulting in an inhibition of T3 degradation. In mammals, birds and fish growth hormone (GH) has been described as a stimulatory agent for ORD activity. In the chick embryo, GH does not increase the amount of T4 ORD but inhibits T3 IRD activity and T3 degradation.

A relationship between circulating natural glucocorticoids and the mechanical responses of the heart in atricial and precocial rodents

1. 1. A comparison was made of the mechanical performance of heart muscle from mouse, an atricial mammal, with corticosterone as glucocorticoid and spiny mouse ( Acomys cahirinus), a precocial mammal, with cortisol as glucocorticoid. 2. 2. Force-frequency responses were negative in mouse and positive in spiny mouse. 3. 3. During recovery, there was a gradual increase and an overshoot in the mouse, while in the spiny mouse there was an initial enhanced response, diminishing gradually with time. 4. 4. High calcium concentration inhibited contractile tension in mouse heart, while it was positively inotropic in spiny mouse heart. Changes in the concentration of calcium did not change the patterns of force-frequency response. 5. 5. Lowering the experimental temperature increased the time course and amplitude of the tension curve. However, various parameters exhibited different temperature sensitivity. 6. 6. There was a significant difference in the levels of circulating cortisol between male and female spiny mice. 7. 7. It is proposed that the differences in the mechanical responses of mouse and spiny mouse hearts may be explained in terms of the effects of the specific glucocorticoid hormone on the development of the sodium-calcium exchanger.

Altricial and precocial mammals: A model of neural and muscular development

AbstractThis model of growth offers a quantitative definition for altricial and precocial newborns, makes muscular strength a benchmark for locomotor independence, and discriminates related genera as well as genera across major taxonomic divides. The model contrasts four theoretical conditions of the neonate (I, small brain, weak musculature; II, small brain, strong musculature; III, large brain, weak musculature; IV, large brain, strong musculature) with species from three orders of placental mammal. Each species exhibits a distinct mother‐infant strategy from the altricial red panda cub (condition I) and the golden lion tamarin (condition III) to the precocial wildebeest calf (condition IV). The model proposes that early growth rates of brain and muscle correlate with nutrition, maternal effort during gestation and lactation, and parental care, whereas postnatal muscular growth correlates directly with adult body size and locomotor repertoire. An example of condition II (small brain, strong musculature) has not been found. This suggests that muscle does not grow in advance of the brain and that the brain acts as a pacemaker of growth. In order to increase our understanding of exotic species, noninvasive measures (body weight and length) and observations (opening of the eyes and ears, hair density, weaning, and the abilities to ther‐moregulate and to move) should be supplemented with analysis of the differential tissue and organ growth. In both theoretical and practical ways analysis of deceased individuals contributes to the understanding of all species.

Postnatal Variation in Metabolism and Body Temperature in a Precocial Lagomorph

1. This paper explores the relationship between energy expenditure, body size and the capacity for homeothermy in young of a precocial mammal. 2. Metabolism and rectal temperature (T b ) were measured during postnatal development in 4-81-day-old white-tailed jackrabbits (Lepus townsendii). 3. Whole-animal metabolism increased with age, mass-specific metabolism decreased with age, and mass-independent metabolism showed no age-related change. 4. Jackrabbits 4-5 days old responded to low ambient temperature (T a ) by increasing metabolism, but nonetheless, their T bS declined at low T a

Comparative Reproductive Strategies of Altricial and Precocial Eutherian Mammals

Mammals produce neonates of varying degrees of development described by the terms altricial and precocial. I rank eutherian mammals by a comprehensive measure of development in which neonates are scored in four areas of independence: thermoregulatory, sensory, locomotory and nutritional. The association between neonatal development and nine life-history traits is examined in 239 species. The distribution of neonatal developmental rankings is associated with adult mass and is related to taxonomic level, with precocial neonates more common among orders, and altricial neonates more common among genera and species. When the effect of adult mass is controlled, precocial mammals produce heavier neonates and heavier litters, possess longer gestation periods, attain adult mass more slowly, and have smaller litter sizes. Mass at weaning, length of the total reproductive interval, and age at first parturition do not differ among developmental categories. Although the continuous nature of development is intuitively appealing, mammalian development patterns do not map onto predictable, continuous changes in life-history patterns. Length of the lactation period is extended in precocial primates but shortened in precocial rodents. Neonate mass varies continuously with stage of neonatal development, while litter size varies dichotomously, and age at first parturition and litter mass differ uniquely in only one developmental category. Thus, neonatal developmental patterns do not appear to result from one continuous axis of selection.

The developmental emergence of a map of auditory space in the superior colliculus of the guinea pig

We describe the developmental emergence of a topographically ordered map of auditory space in the deep layers of the guinea pig superior colliculus. The central auditory system of this precocial mammal is functional in utero. A map of auditory space in the superior colliculus is not, however, electrophysiologically demonstrable until 32 days after birth (DAB). The map develops in 4 postnatal phases. In very young animals (1–15 DAB) vigorous responses to auditory stimuli were recordable from collicular sites. Apart from a preference for stimuli originating in the contralateral hemifield of auditory space, the responses in these young animals, however, showed little evidence of directional tuning. In animals aged between 16 and 30 DAB, an increasing proportion of responses displayed directional tuning but such responses were not arranged so as to constitute a topographic map. A relatively short third developmental phase (31–32 DAB) involved the ordering of individually tuned responses so as to form a topographic map of the contralateral auditory hemifield. As the animals further mature the individual responses display a higher degree of spatial tuning reflecting an ongoing process of refinement.

Reproductive strategies, body size, and encephalization in primate evolution

In order to understand fully the generally high level of encephalization observed in living primates, we must determine why early primates exhibited moderately large relative brain sizes compared to their early Tertiary contemporaries. The relatively high degree of encephalization in early primates may be related at least in part to the fact that they were highly unusualamong mammals in combining a small body size with a strongly precocial reporductive strategy. Other small, precocial mammals also exhibit moderately high levels of encephalization; but primates appear to have been truly uniquein being the only such small-sized and highly precocial group to give rise to extensive radiations of larger descendants. This is a key element in understanding primate brain evolution, because the initial “head start” of the early primates was translated up to larger sizes in descendants. The possible relationships among encephalization, precociality, small size, and arboreality are discussed, particularly in light of recent debates concerning the validity of the superorder Archonta. This work emphasizes that we need to consider relative brain size as but one element in a complex synergistic network of morphological and life-history features.

Brain size, development and metabolism in birds and mammals

Recent hypotheses that variation in brain size among birds and mammals result from differences in metabolic allocation during ontogeny are tested.Indices of embryonic and post‐embryonic brain growth are defined. Precocial birds and mammals have high embryonic brain growth indices which are compensated for by low post‐embryonic indices (with the exception of Homo supiens). In contrast, altricial birds and mammals have low embryonic and high post‐embryonic indices. Altricial birds have relatively small brains at hatching and develop relatively large brains as adults, but among mammals there is no equivalent correlation between variation in adult relative brain sizes and state of neonatal development.Compensatory brain development in both birds and mammals is associated with compensatory parental metabolic allocation. In comparison with altricial development, precocial development is characterized by higher levels of brain growth and parental metabolic allocation prior to hatching or birth and lower levels subsequently. Differences between degrees of postnatal investment by the parents in the young of precocial birds versus precocial mammals may result in the different patterns of adult brain size associated with precociality versus altriciality in the two groups.The allometric exponent scaling brain on body size differs among taxonomic levels in birds. The exponent is higher for some parts of the brain than others, irrespective of taxonomic level. Unlike mammals, the exponents for birds do not show a general increase with taxonomic level. These pattcrns call into question recent interpretations of the allometric exponent in birds. and the reason for changes in exponent with taxonomic level.

Postnatal development of the circadian rhythm of thyrotropic cells in precocial and altricial mammals

Postnatal development of the circadian rhythm of thyrotropic cells in precocial and altricial mammals