Variation in maternal investment in a small cervid; the effects of cohort,sex, litter size and time of birth in roe deer (Capreolus capreolus) fawns

 We investigated the effects of cohort, sex, litter size and time of birth on birth weights and postnatal growth rates of roe deer fawns in a highly reproductive Norwegian population. By repeatedly recapturing radio-collared individuals, a total of 950 weights were obtained from 231 fawns of known age. In accordance with earlier studies, there was a period of linear growth during the first month following birth. Mean postnatal growth rates of 155 g/day are the highest yet recorded for roe deer; however, the mean birth weights of fawns were lower than those reported from populations in continental Europe. During the period of linear growth, we found no sex differences. However, growth rates were affected both by time of birth and litter size; fawns born early had lower growth rates than fawns born during or after the peak calving period, and fawns in triplet – groups had lower growth rates than either fawns in twin – groups or single fawns. Despite a fourfold increase in population density during the study, this factor was not able to explain variation in postnatal growth rates, although cohort effects on birth weight were evident. Received: 13 May 1996 / Accepted: 26 June 1996     

Placental restriction of fetal growth reduces size at birth and alters postnatal growth, feeding activity, and adiposity in the young lamb

Intrauterine growth restriction (IUGR) is associated with accelerated growth after birth. Together, IUGR and accelerated growth after birth predict reduced lean tissue mass and increased obesity in later life. Although placental insufficiency is a major cause of IUGR, whether it alters growth and adiposity in early postnatal life is not known. We hypothesized that placental restriction (PR) in the sheep would reduce size at birth and increase postnatal growth rate, fat mass, and feeding activity in the young lamb. PR reduced survival rate and size at birth, with soft tissues reduced to a greater extent than skeletal tissues and relative sparing of head width (P < 0.05 for all). PR did not alter absolute growth rates (i.e., the slope of the line of best fit for age vs. parameter size from birth to 45 days of age) but increased neonatal fractional growth rates (absolute growth rate relative to size at birth) for body weight (+24%), tibia (+15%) and metatarsal (+18%) lengths, hindlimb (+23%) and abdominal (+19%) circumferences, and fractional growth rates for current weight (P < 0.05) weekly throughout the first 45 days of life. PR and small size at birth reduced individual skeletal muscle weights and increased visceral adiposity in absolute and relative terms. PR also altered feeding activity, which increased with decreasing size at birth and was predictive of increased postnatal growth and adiposity. In conclusion, PR reduced size at birth and induced catch-up growth postnatally, normalizing weight and length but increasing adiposity in early postnatal life. Increased feeding activity may contribute to these alterations in growth and body composition following prenatal restraint and, if they persist, may lead to adverse metabolic and cardiovascular outcomes in later life.     

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

In the absence of processes regulating morphogenesis and growth, phenotypic variance of a population experiencing no selective mortality should increase throughout ontogeny. To determine whether it does, we measure variance of skull shape using geometric morphometrics and examine its ontogenetic dynamics in the precocial cotton rat (Sigmodon fulviventer) and the altricial house mouse (Mus musculus domesticus). In both species, variance of shape halves between the two youngest samples measured (between 1 and 10 days postnatal and 10 and 15 days postnatal, respectively) and thereafter is nearly constant. The reduction in variance did not appear to result from a general regulation of skull size or developmental timing, although skull size may also be regulated and developmental timing is an important component of the variation in skull shape of young house mice. The ontogenetic dynamics of variance suggest two possible scenarios. First, variation generated during fetal or early postnatal growth is not immediately compensated and therefore accumulates, whereas later in growth, variation is continually generated and rapidly compensated. Second, variation generated during fetal and early postnatal growth is rapidly compensated, after which no new variance is produced. Based on a general model for bone growth, we hypothesize that variance is generated when bone grows under the direction of disorganized muscular movements and decreases with increasing neuromuscular control. Additionally, increasing coherence of signals transmitted by the growing brain and sensory organs, which exert tensile forces on bone, may also canalize skull shape.     

A comparative study of embryonic development of some bird species with different patterns of postnatal growth

Some studies show that birds with high postnatal growth rates (e.g. altricial species) are characterized by a rapid early development of "supply" organs, such as digestive organs. Birds with low postnatal growth rates (e.g. precocial species) exhibit a slower early development of these organs and a more rapid early development of other "demand" organs, such as brain, muscles, skeleton and feathers. To test whether these differences can be traced back to early embryonic development and whether they can be associated with changes in developmental timing, i.e. heterochrony, we compared embryos of the precocial quail and the altricial fieldfare, two bird species with low and high postnatal growth rates, respectively. We used classical staging techniques that use developmental landmarks to categorize embryonic maturity as well as morphological measurements. These techniques were combined with immune detection of muscle specific proteins in the somites. Our data showed that the anlagen of the head, brain and eyes develop earlier in the quail than in the fieldfare in contrast to the gut which develops earlier in the fieldfare than in the quail. Our data also showed that the quail and the fieldfare displayed different rates of myotome formation in the somites which contribute to muscle formation in the limbs and thorax. We believe these observations are connected with important differences in neonatal characteristics, such as the size of the brain, eyes, organs for locomotion and digestion. This leads us to the conclusion that selection for late ontogenetic characteristics can alter early embryonic development and that growth rate is of fundamental importance for the patterning of avian embryonic development. It also appears that this comparative system offers excellent opportunities to test hypotheses about heterochrony.     

Allometric study of the lachrymal and Harderian glands of the rat during postnatal life.

The authors performed an allometric study of the growth of the rat's lachrymal and Harderian glands, during postnatal life. From the analysis of the results, they could conclude: (1) the growth of these glands in relation to body weight, during postnatal life, could be considered similar, following the allometric law; (2) the differential growth of the glands occurred in two stages: from birth until the 15th day and from the 15th day until the final period of life studied; (3) the two stages of development were separated by a critical period, during which an abrupt modification of the allometric coefficient occurred; (4) during the first days of postnatal life, the development of the Harderian gland was characterized by a high rate of growth and, just after eyelid disjunction and during rest of postnatal life, by a rate of allometric of growth less than 1. It is interesting to observe that the lachrymal and Harderian glands' critical period of development on the 15th day of postnatal life coincides with the time at which the eyelids of the animal open.     

Phylogenetic implications of comparative primate growth rates

Growth data from a number of species of Old and New World primates have been analyzed by calculating instantaneous relative growth rates. Species discussed are the New World species Saimiri sciureus and Saguinus nigricollis, and the Old World species Pan troglodytes and Macaca mulatta. The analysis of the perinatal growth data indicated that differences in relative growth rates are present during early periods of growth. More specifically, it was found that the closer taxonomically a species is to man the greater the deceleration of growth during the first postnatal year. It is suggested that this may be a general primate trend.     

Studies on the mechanisms of histidase development in rat skin and liver. II. Alterations in enzyme levels and synthetic rates during development.

The divergent postnatal developmental courses of histidase catalytic activity in rat liver and skin of the same animals, viz., a progressive rise in hepatic enzyme activity and a simultaneous decline in epidermal activity, has been shown to be accompanied by corresponding alterations in the quantities of the same enzyme protein. These tissue specific developmental changes in enzyme amount have been shown, furthermore, to be a result of selective parallel alterations in histidase synthetic rates. Rates of [³H]leucine incorporation into histidase, isolated by immunoprecipitation, relative to incorporation rates into total soluble tissue protein, increase in liver, while simultaneously decreasing in skin of the same animals during postnatal development.     

The origin of eutherian mammals

Palaeontologically recognizable eutherians originated no later than the Early Cretaceous in warm, probably moderately seasonal climates. Immediate ancestors were small, sharing many anatomical, physiological and reproductive features with small modern marsupials. Development of characteristically eutherian features involved interactions of body size, rates of metabolism, energetic costs of reproduction, anatomical/physiological processes of development and effects of each upon rates of population growth. In contrast to eutherians, marsupials have a narrow range of basal metabolic rates (lacking high rates), and show no direct links between rate of energy expenditure and gestation period, postnatal growth rate, fecundity or reproductive potential. Biological implications of this contrast are most pronounced at small body sizes. When resources are abundant, the relatively higher growth rates and earlier maturation of small eutherians (particularly those with high rates of metabolism) can lead to rapid population growth; among most marsupials, however, both pre- and postnatal constraints apparently preclude attainment of such high rates of reproduction. Also, only eutherians among the amniotes combine intimacy of placentation with prolonged active intra-uterine morphogenesis. Once established, that combination permitted (and even favoured) increases in diversity of adaptation in such disparate aspects as elevated metabolic rate, increased pre- and postnatal growth rates, increased encephalization, greater longevity, increased gregariousness, greater karyotypic flexibility, and augmented variability in adult morphology. However, all such boosts in diversity were probably secondary and dependent upon prior innovation of trophoblastic/uterine wall immunological protection of foetal tissues during prolonged intra-uterine development. Increased metabolic rates followed thereafter, with synergisms that may have speeded evolution among early eutherians. Eutherian-style trophoblast probably originated in the Mesozoic. Dependent adaptations, variably expressed, evolved later in sundry descendant lineages. Reproductive differences between marsupials and eutherians are not biologically trivial; to the contrary, breakthroughs among eutherians assured their dominance: (1) in high intensity food habits; (2) at small body masses; and (3) in very cold climates.     

A Genetic Analysis of Targeted Growth in Mice

Effects of normal growth regulation on components of phenotypic variance and covariance of body weight were examined in a cross-fostering study of growth between 2 and 10 wk of age in ICR randombred mice. Different early growth rates caused genetic, postnatal maternal and residual environmental variances to increase, but these variances were subsequently reduced by negative autocorrelation between early and later growth. Postnatal maternal variance continued to increase for about 1 wk after weaning but then decreased substantially. Genetic variance caused by preweaning growth followed a pattern of increase and decrease very similar to that of postnatal maternal variance, but this pattern was masked by new genetic variance. Normal growth regulation affects the magnitudes of genetic variances and serial autocorrelations. The timing of these changes suggests that regulation of cell numbers reduces variance near the end of exponential growth, but this may be obscured by subsequent increase in cell size. In contrast with earlier studies, we find that targeted growth reduces both genetically and environmentally determined differences among early growth trajectories. Final size may be determined by an antagonistic balance between early growth rate and age at initiation of puberty.     

Pre- and postnatal growth of the Cape porcupine Hystrix africaeaustratis

Pre- and postnatal growth of the Cape porcupine Hystrix africaeaustralis is evaluated by means of the Huggett & Widdas equation, a modification thereof, and the von Bertalanffy equation. Specific foetal growth velocity for the Cape porcupine is higher than that recorded for most other hystricomorph rodents, but similar to that recorded for large-bodied rodents of the same group. Relatively high foetal growth velocity in porcupines is ascribed to their relatively short gestation period, the latter being longer than expected for mammals of equal size, but shorter than expected for a hystricomorph rodent.
Postnatal growth is nearly linear up to the age of 20 weeks and asymptotic body weight is attained at an age of 52 weeks, this coinciding with the observed age at sexual maturity. Growth rates of males and females are similar. Their high rate of postnatal growth and development results in an extended reproductive period, thereby enhancing individual reproductive values by counteracting the effects of seasonal breeding and small litter size.     

Contribution on the physiological heart growth. (Experimental autoradiographic studies in mice)]

After injections of 3H thymidine or 3H proline, the physiological hearth growth in mice of the CBA strain belonging to various age groups was studied by means of autoradiography. The most important results are the following: The duration of the postnatal growth period is determined by the degree of maturity of the heart at the time of birth. It varies from species to species. 2. In the perinatal developmental phase the percentage of the 3H thymidine-labelled connective-tissue nuclei is higher than that of the muscle nuclei. In this period the connective supporting tissue is considerably strengthened. 3. During the postnatal developmental phase the DNA synthesis in the muscle nuclei aids the preparation of mitoses. After the postnatal duplication of cells the mitotic genes are repressed. The further growth is effected by the increase in weight of the individual fibres. 4. The process of growth is substantially determined by the intracardiac or intramyocardiac pressure and thus by the extension of the muscle fibre. Prior to birth the percentage of the labelled nuclei of muscle cells and connective tissue cells in the right ventricle was higher than in the left ventricular wall. In the postnatal period we observed a shift in the percentage of the labelled cells towards the left ventricular wall. The basis and the median section of the ventricular wall. The basis and the median section of the ventricular wall contain a higher percentage of labelled cells than does the apex cordis. During the first two weeks of live most of the DNA synthesising nuclei of muscle and connective tissue cells are localized in the two inner muscle shells. Later in life no clear distinctions can be demonstrated between the individual ventricular layers.     

Direct genetic and postnatal maternal genetic effects on body composition in mice selected for body weight.

Line crossfostering techniques were used to study differences among selected and control lines of mice in direct genetic and postnatal maternal genetic influences on preweaning (day 12) body weight and composition. The lines were selected for high (H6) and low (L6) 6-week body weight and the control line (C2) was maintained by random selection. There were positive correlated responses to selection in both direct genetic and postnatal maternal genetic effects on body weight and weights of all body components (P less than 0.01) except for water and ash weight in H6. The correlated responses in postnatal maternal genetic effects were of the same order of magnitude as those in direct genetic effects. Correlated responses were greater in L6 than in H6. Correlated responses in direct genetic effects were positive (P less than 0.01) for water percent in H6 and ether extract percent in L6, and negative (P less than 0.01) for water percent and lean percent in L6. Correlated responses in postnatal maternal genetic effects were positive for ether extract percent and negative for water percent (P less than 0.01). Correlated responses were far greater in L6 than in H6 and were greater for postnatal maternal genetic effects than for direct genetic effects. Analyses of covariance results indicated line differences in the relative growth rates of the body components.     

Agrin is highly expressed by chondrocytes and is required for normal growth

Agrin is a heparan sulfate proteoglycan that is best known for its crucial involvement in the organization and maintenance of postsynaptic structures at the neuromuscular junction. Consistent with this role, mice deficient of agrin die at birth due to respiratory failure. Here we examined the early postnatal development of agrin-deficient mice in which perinatal death was prevented by transgenic expression of neural agrin in motor neurons. Such transgenic, agrin-deficient mice were born at Mendelian ratio but exhibited severe postnatal growth retardation. Growth plate morpholgy was markedly altered in these mice, with changes being most prominent in the hypertrophic zone. Compression of this zone was not caused by reduced viability of hypertrophic chondrocytes, as no differences in the apoptosis rates could be observed. Furthermore, deposition of the major cartilage matrix components collagen type II and aggrecan was slightly reduced in these mice. Consistent with a role for agrin in skeletal development, we show for the first time that agrin is highly expressed by chondrocytes and localizes to the growth plate in wild-type mice. Our data show that agrin is expressed in cartilage and that it plays a critical role in normal skeletal growth.     

Size at birth, postnatal growth and risk of obesity

Epidemiological studies over the last 15 years have shown that size at birth, early postnatal catch-up growth and excess childhood weight gain are associated with an increased risk of adult cardiovascular disease and type 2 diabetes. At the same time, rising rates of obesity and overweight in children, even at pre-school ages, have shifted efforts towards the identification of very early factors that predict risk of subsequent obesity, which may allow early targeted interventions. Overall, higher birth weight is positively associated with subsequent greater body mass index in childhood and later life; however, the relationship is complex. Higher birth weight is associated with greater subsequent lean mass, rather than fat mass. In contrast, lower birth weight is associated with a subsequent higher ratio of fat mass to lean mass, and greater central fat and insulin resistance. This paradoxical effect of lower birth weight is at least partly explained by the observation that infants who have been growth restrained in utero tend to gain weight more rapidly, or 'catch up', during the early postnatal period, which leads to increased central fat deposition. There is still debate as to whether there are critical early periods for obesity: does excess weight gain during infancy, childhood or even very early neonatal life have a greater impact on long-term fat deposition and insulin resistance? Early identification of childhood obesity risk will be aided by identification of maternal and fetal genes that regulate fetal nutrition and growth, and postnatal genes that regulate appetite, energy expenditure and the partitioning of energy intake into fat or lean tissue growth.     

Myofibrillar protein turnover. Synthesis rates of myofibrillar and sarcoplasmic protein fractions in different muscles and the changes observed during postnatal development and in response to feeding and starvation.

Measurement of rates of synthesis of skeletal-muscle proteins in adult rats shows that the faster overall rate of turnover in diaphragm and soleus muscles compared with several other, more glycolytic, muscles is also exhibited by the myofibrillar proteins, since the ratio of sarcoplasmic to myofibrillar protein synthesis is similar for all muscles. Further, throughout postnatal development, when the overall turnover rate falls with age, parallel changes occur for the myofibrillar proteins, as indicated by a constant ratio of sarcoplasmic to myofibrillar protein synthesis (2.06) in the steady state after overnight starvation. Only in the youngest (4 weeks old) rats is a slightly lower ratio observed (1.72). These results indicate that, when changes in the overall turnover rate of muscle proteins occur, the relative turnover of the two major protein fractions stays constant. However, measurements in the non-steady state during growth and after starvation for 4 days show that the relative synthesis rates of the two fractions change as a result of a disproportionate increase in myofibrillar protein synthesis during growth and decrease during starvation. Thus the synthesis rate of the slower-turning-over myofibrillar protein fraction is more sensitive to nutritional state than is that of the sarcoplasmic protein. It is suggested that such responses may help to maintain constant tissue composition during non-steady-state conditions of growth and atrophy.     

Abnormalities in the cell-division cycle in Roberts syndrome fibroblasts: a cellular basis for the phenotypic characteristics?

Roberts-SC phocomelia syndrome (RS) is a recessively inherited developmental disorder characterized by profound pre- and postnatal growth reduction, symmetrical limb reductions of varying severity, and craniofacial abnormalities. Many patients with RS exhibit a striking chromosomal abnormality involving the heterochromatic, C-banding regions of most chromosomes. Dermal fibroblast strains from three such patients were used to investigate in vitro cellular growth characteristics. Plating efficiency, colony-forming ability, and cell density at confluence in RS were compared with dermal fibroblast strains from pediatric patients without RS and fetal lung fibroblast strains. Time-lapse cinematography was used to study mitotic duration and cytokinesis in RS and various control fibroblast strains. Clearly, cell from affected individuals had deficiencies that led to a multitude of abnormalities at the cellular level. These included: abnormal mitosis and cytokinesis, reduced cell growth, atypical cell morphology, and altered chromosomal morphology at peri- and paracentromeric and nucleolar-organizing regions. These findings suggest that the basis for at least some of the phenotypic abnormalities characteristic of this trait may reside in the reduced growth rates of the cells during the course of development. This could account for the reduced pre- and postnatal growth rates as well as for the developmental abnormalities, since deficiencies of cells in developing anlagen could well lead to alterations in developmental patterns.     

Developmental constraints on limb growth in domestic and some wild canids

The domestic dog varies remarkably in limb size. Presumably, such differences in limb size stem from inequities in postnatal specific growth rate. I test this hypothesis by examining the postnatal growth of limb bones (40–250 days post-partum) in four dog breeds of dramatically different adult size; Lhasa Apso, Cocker Spaniel, Labrador Retriever and Great Dane. The results show that the limb bones of these four breeds have similar specific growth rates throughout most of postnatal development. Thus, proportionate differences in limb bone length are established during perinatal growth (0–40 days post-partum) or before birth.
Comparisons of postnatal growth in the Great Dane and two wild canids of dramatically different leg length, the Bush dog ( Speothos venaticus ) and the Maned wolf ( Chrysocyon brachyurus ) also show a near congruency of specific growth rate curves. However, despite these similarities, the adult limb proportions of small dogs and small wild canids are different. Dogs also differ from wild canids in the relative variability of gestation time. All dogs have a similar gestation period of 60–63 days which is independent of birth weight, whereas the two are directly related in wild canids. I suggest that small dogs may differ in limb proportions from small wild canids because the latter have a shorter gestation period. Thus, the relative invariability of gestation time in domestic dogs may act as a fundamental constraint on their morphologic variability.     

Growth,development, and parental care in the western tarsier (Tarsius bancanus) in captivity: Evidence for a “slow” life-history and nonmonogamous mating system

I studied reproduction, prenatal and postnatal growth rates, behavioral ontogeny, and parental care in nine captive births to two wild-caught pairs of Tarsius bancanusover a 5-year period. T. bancanusinvariably gives birth to a single infant of approximately 20% maternal body mass after an extremely long gestation period. The fetal growth rate is among the slowest recorded for any mammal and the relative postnatal growth rate to physical maturity is the lowest in a sample of 26 prosimian species examined. These life-history variables, and a slow rate of reproduction, contribute to an extremely low г _max in this and other species of Tarsius.The relative rate of behavioral development, especially foraging and locomotor behaviors, is extremely rapid for a specialized predator. Infants attained nutritional independence at approximately 80 days and perfected hunting skills without apparent help from either parent. Mothers were very protective of their young and kept fathers from having contact with infants through heightened agonism after birth, and thus , there was no evidence of direct paternal care. The data suggest that there is an energetic/dietary basis for slow pre- and postnatal growth rates, but an extremely large neonatal brain size enables the rapid behavioral development and neuromuscular coordination necessary for this specialized predator to attain early nutritional independence. The captive and field data also suggest that extremely restrictive conditions exist for the purported monogamous mating system of T. bancanusand that an alternative mating system is more likely.