Orthocephalization in the postweaning squirrel monkey

Twenty male squirrel monkeys (Saimiri sciureus boliviensis) raised in captivity were allotted to one of the following groups: weanling control (C6) sampled at 6 months of age; young control (C24) fed ad libitum on a control diet and killed at 24 months of age; and malnourished (M24) fed ad libitum on a low-protein diet and sampled at 24 months of age. Cranial points and the lateral semicircular canals were marked. On each skull, a strict lateral teleradiograph was taken, and the lengths of the midsagittal chords and their angles with respect to the vestibular line were measured. Age changed the lengths in about 70% of the chords and more than 50% of the angles. Malnutrition arrested about 50% of the lengths, but the angles were practically not affected. It is concluded that the postweaning Saimiri sciureus undergoes orthocephalization according to a general pattern already observed in rodents and suggested for pongids. Postweaning malnutrition affected growth in size but not shape changes related to the orthocephalization of the Saimiri skull. © 1996 Wiley-Liss, Inc.     

Effect of diet and starvation on the activity state of branched-chain 2-oxo-acid dehydrogenase complex in rat liver and heart

In rats fed a high-protein diet, the branched-chain 2-oxo-acid dehydrogenase complex in liver was essentially fully acitve and its activity state was unaffected by subsequent starvation for 48 h. Feeding with a low-protein diet led to a decrease in the activity state which was essentially reversed by 48 h of starvation. In heart, the enzyme was primarily inactive (activity state 18%) in rats fed a high-protein diet, with both low-protein diet and starvation leading to a further decrease in the activity state.     

Dispelling dog dogma: an investigation of heterochrony in dogs using 3D geometric morphometric analysis of skull shape

Heterochrony is an evolutionary mechanism that generates diversity via perturbations of the rate or timing of development that requires very little genetic innovation. As such, heterochrony is thought to be a common evolutionary mechanism in the generation of diversity. Previous research has suggested that dogs evolved via heterochrony and are paedomorphic wolves. This study uses three-dimensional landmark-based coordinate data to investigate heterochronic patterns within the skull morphology of the domestic dog. A total of 677 adult dogs representing 106 different breeds were measured and compared with an ontogenetic series of 401 wolves. Geometric morphometric analysis reveals that the cranial shape of none of the modern breeds of dogs resembles the cranial shapes of adult or juvenile wolves. In addition, investigations of regional heterochrony in the face and neurocranium also reject the hypothesis of heterochrony. Throughout wolf cranial development the position of the face and the neurocranium remain in the same plane. Dogs, however, have a de novo cranial flexion in which the palate is tilted dorsally in brachycephalic and mesaticephalic breeds or tilted ventrally in dolichocephalic and down-face breeds. Dogs have evolved very rapidly into an incredibly morphologically diverse species with very little genetic variation. However, the genetic alterations to dog cranial development that have produced this vast range of phylogenetically novel skull shapes do not coincide with the expectations of the heterochronic model. Dogs are not paedomorphic wolves.     

Effect of diet and starvation on the activity state of branched-chain 2-oxo-acid dehydrogenase complex in rat liver and heart

In rats fed a high-protein diet, the branched-chain 2-oxo-acid dehydrogenase complex in liver was essentially fully active and its activity state was unaffected by subsequent starvation for 48 h. Feeding with a low-protein diet led to a decrease in the activity state which was essentially reversed by 48 h of starvation. In heart, the enzyme was primarily inactive (activity state 18%) in rats fed a high-protein diet, with both low-protein diet and starvation leading to a further decrease in the activity state.     

Heterochrony: Developmental mechanisms and evolutionary results

The concept of heterochrony, that the relative timing of ontogenetic events can shift during evolution, has been a major paradigm for understanding the role of developmental processes in evolution. In this paper we consider heterochrony from the perspective of developmental biology. Our objective is to redefine heterochrony more broadly so that the concept becomes readily applicable to the evolution of the full range of ontogenetic processes, from embryogenesis through the adult. Throughout, we stress the importance of considering heterochrony from a hierarchical perspective. Thus, we recognize that a heterochronic change at one level of organization may be the result of non-heterochronic events at an underlying level. As such, heterochrony must be studied using a combination of genetic, molecular, cellular, and morphological approaches.     

Effect of short-term vs. long-term elevation of dietary protein intake on responsiveness of rat thick ascending limbs to peptide hormones

We compared the renal responses of rats on three diet regimens. Rats received either 8% protein food (low-protein, LP) for 10 weeks following weaning, 8% protein for 9 weeks followed by 1 week on 30% protein (short-term high-protein, SHP), or 30% protein for 10 weeks (high-protein, HP). Kidneys from HP rats were enlarged by approximately 50%, or 20% when corrected for body mass. Most of this hypertrophy resulted from enlargement of the inner stripe of the outer medulla, site of the thick ascending limbs (TAL), and TAL from HP rats were larger in diameter. SHP rats had TAL diameters similar to HP rats, but changes in renal mass or height of renal zones did not reach statistical significance. The activity of adenylyl cyclase (AC) in TAL, measured from the accumulation of cAMP in isolated tubules, increased with dose of both arginine vasopressin (AVP) and glucagon in all rats. However, HP rats had significantly higher hormone-induced AC activity than LP or SHP rats, which were not different from each other. Our results suggest that tubule hypertrophy may precede up-regulation of hormone-sensitive AC activity during the progression of renal response to elevated dietary protein.     

Is Sequence Heterochrony an Important Evolutionary Mechanism in Mammals?

It is postulated widely that changes in developmental timing (i.e., heterochrony) represent a major mechanism of evolutionary change. However, it is only with recent methodological advances that changes in the order in which development proceeds (sequence heterochrony) can be identified and quantified. We apply these techniques to examine whether heterochrony in the early embryonic (organogenetic) period has played an important role in the diversification of mammals. Although we find clear instances of sequence heterochrony in mammals, particularly between eutherians and marsupials, the majority of mammalian lineages that we could examine (those within the major clades Euarchontoglires and Laurasiatheria) show few or no heterochronic changes in the 116 events examined (e.g., Artiodactyla, Euarchonta, Fereuungulata, Glires, Primates, Rodentia). This is in contrast with the timing shifts reported between and within other tetrapod clades. Our results suggest that sequence heterochrony in embryonic stages has not been a major feature of mammalian evolution. This might be because mammals, and perhaps amniotes in general, develop for an extended time in a protected environment, which could shield the embryos from strong diversifying selection. Our results are also consistent with the view that mammal embryos are subject to special developmental constraints. Therefore, other mechanisms explaining the diversity of extant mammals must be sought.     

Physiological and biochemical responses to dietary protein in the omnivore passerine Zonotrichia capensis (Emberizidae)

We studied the physiological, biochemical and morphological responses of the omnivore sparrow Zonotrichia capensis, a small opportunistic passerine from Central Chile acclimated to high- and low-protein diets. After 4 weeks of acclimation to 30% (high-protein group) or 7% (low-protein group) dietary casein, we collected urine and plasma for nitrogen waste production and osmometry analysis, and measured gross renal morphology. Plasma osmolality and hematocrit were not significantly affected by dietary treatment, but urine osmolality was higher in the high-protein group than in the low-protein group. Kidney and heart masses were higher in animals acclimated to the high-protein diet. Mean total nitrogen waste was significantly higher in the high-protein group, but the proportions of nitrogen excreted as uric acid, urea and ammonia were unaffected by diet. Our data suggest that the response of Z. capensis to an increase in dietary protein content is through greater amounts of total nitrogen excretion and hypertrophy of kidney structures, without any modification of the proportion of excretory compounds.     

Patterns and mechanisms of growth of fifth-instar Manduca sexta caterpillars following exposure to low- or high-protein food during early instars.

For many insect herbivores, variation in protein availability is a pervasive part of the environment. I explore how variable protein availability affects growth rates of fifth-instar Manduca sexta caterpillars and how growth is related to behavior and physiology. Groups of larvae were reared on low- or high-protein artificial diets (5.9% and 17.7% casein by dry weight, respectively) and then transferred in the fifth instar to the same or opposite diet. During or after the 24-h period following transfer, I measured growth rate, consumption rate, growth efficiency, midgut proteolytic activity, and masses of midgut contents and tissues. Fifth-instar caterpillars reared in earlier instars on high-protein diet grew about 20% more rapidly over 24 h than did caterpillars reared on low-protein diet. This growth pattern appears to be caused by differences in consumption and growth efficiency: caterpillars reared on high protein consumed more food, and used it more efficiently, than did caterpillars reared on low-protein diet. Over the short term (24 h), in contrast, fifth instars that received low-protein diet grew as rapidly as caterpillars that received high-protein diet. Increased (compensatory) consumption appears to be the primary mechanism by which caterpillars consuming low-protein food maintained growth rates.     

Differential modulation of dopaminergic systems in the rat brain by dietary protein

Rats that consume a diet 50% rich in protein exhibit hyperactivity and hyperresponsiveness to nociceptive stimuli, in which facilitation of dopaminergic activity has been implicated. We studied the regional changes in the concentrations of dopamine (DA) and its metabolites, dihydroxyphenylacetic acid (DOPAC) and homovanillic acid (HVA) in the brains of rats that were maintained on high-protein (HP, 50% casein), normal-protein (NP, 20% casein), and low-protein (LP, 8% casein) diets for 36 weeks. Brain nuclei that represented different DAergic systems were punchdissected and analyzed using HPLC. In the substantia nigra, the striatum, and the dentate gyrus, DA concentrations decreased and increased, respectively, with a decrease and increase in dietary protein (p<0.05 compared to the NP diet). Similar trends in the effect of the HP diet were observed in the ventral tegmental area, amygdala, frontal cortex, subiculum, centromedial nucleus (CM) of the thalamus, and inferior colliculi (IC), although the differences in DA concentrations were not statistically significant. These brain areas also showed a pattern of decreased DA concentration in association with the LP diet, and the differences were statistically significant (p<0.05) in the CM and IC. DA concentrations in most regions of the midbrain and brainstem were not different between the diet groups, nor were consistent trends observed in those regions. Also, there were no consistent relationships between DOPAC/DA and HVA/DA ratios and dietary protein level. These data suggest that only discrete dopaminergic neuronal circuits in the rat forebrain were sensitive to changes in dietary protein level.     

The genetic control of heterochrony: Evidence from developmental mutants of Pisum sativum L.

Heterochrony, as a means of evolution in which the rate or timing of developmental events of the descendant is altered compared with that of the ancestor, is of significance because it suggests that rapid and dramatic morphological changes are possible with few genetic changes. The putative origin of plant taxa by this means of evolution is becoming increasingly frequent in the literature but there is little evidence of the extent of the genetic change necessary to alter the timing of developmental events to produce such changes. This study shows that the onset of flowering can be altered independently from the vegetative transition in leaf form in at least one genotype of Pisum in response to different environments. Further, it identifies 9 mutations that act in a heterochronic manner to produce dramatic morphological changes that can be described as progenesis, neoteny, hypermorphosis or acceleration. In addition, it is demonstrated that the same heterochronic process (e.g. progenesis) may be caused by genes controlling distinctly different physiological processes. It is suggested that Pisum is an ideal model species for studies of heterochrony and that few genetic changes are necessary to bring about dramatic heterochronic changes.     

The mechanisms of morph determination in the amphipod Jassa: implications for the evolution of alternative male phenotypes

The proximal basis for and the maintenance of alternative male reproductive strategies and tactics are generally not understood in most species, despite the occurrence of male polymorphism across many taxa. In the marine amphipod Jassa marmorata, males differ in morphology as well as behaviour. This dimorphism corresponds to two contrasting reproductive strategies: small sneaker males or 'minors', and large fighter males or 'majors'. This study uses quantitative genetic analyses in conjunction with experimental manipulations to assess the relative importance of genetic versus environmental factors in the determination and maintenance of these alternative mating strategies. Heritability analyses indicated the reproductive phenotypes do not reflect genetic differences between dimorphic males. By contrast, morph determination was significantly affected by diet quality. Majors essentially only developed on high-protein diets. Field studies also identified a strong correlation between seasonal shifts in the relative proportions of morphs and changes in food (i.e. phytoplankton) quantity and composition, corroborating that diet cues the switch between alternative reproductive tactics. Moreover, the comparison of major and minor growth trajectories identified a heterochronic shift in maturation times between morphs, indicating that ecological selective pressures, rather than just sexual selection, may be involved in the maintenance of this conditional strategy.     

Heterochrony in plant evolutionary studies through the twentieth century

The evolution of plant morphology is the result of changes in developmental processes. Heterochrony, the evolutionary change in developmental rate or timing, is a major cause of ontogenetic modification during evolution. It is responsible for both interspecific and intraspecific morphological differences. Other causes include heterotopy, the change of structural position, and homeosis, the replacement of a structure by another. This paper discusses and reviews the role of heterochrony in plant evolution at the organismal, organ, tissue, cellular, and molecular levels, as well as the relationships among heterochrony, heterotopy, and homeosis. An attempt has been made to include all published studies through late 1999. It is likely that most heterochronic change involves more than one of the six classic pure heterochronic processes. Of these processes, we found neoteny (decreased developmental rate in descendant), progenesis (earlier offset), and acceleration (increased rate) to be more commonly reported than hypermorphosis (delayed offset) or predisplacement (earlier onset). We found no reports of postdisplacement (delayed onset). Therefore, although rate changes are common (both neoteny and acceleration), shifts in timing most commonly involve earlier termination in the descendant (progenesis). These relative frequencies may change as more kinds of structures are analyzed. Phenotypic effects of evolutionary changes in onset or offset timing can be exaggerated, suppressed, or reversed by changes in rate. Because not all developmental changes responsible for evolution result from heterochrony, however, we propose that plant evolution be studied from a viewpoint that integrates these different developmental mechanisms.     

The effects of nutritional status of rabbits and sheep on their resistance to the ticksRhipicephalus evertsi evertsi andR. appendiculatus

Rabbits and sheep were exposed to low-and high-protein diets and subsequently infested three times with adults ofRhipicephalus appendiculatus andRhipicephalus evertsi evertsi. The mean weight ofR.e. evertsi females which dropped from rabbits maintained on a high-protein diet decreased from 515.0±24.9 mg (naive) to 381.5±25.0 (second infestation) to 340.3±23.3 mg (third infestation) while the weight of ticks fed on animals which were exposed to a low-protein diet did not change significantly (2.7%). The mean weight of engorged females ofR. appendiculatus which completed their blood meal on rabbits (high protein) decreased from 520.9±31.8 (naive) to 369.3±39 mg (3rd infestation), a significant decrease of 29.1% compared to a 12.3% decrease in weight between the 1 st and 3rd infestation of females fed on animals on a low-protein diet.Rhipicephalus e. evertsi fed on sheep exhibited the same phenomenon. The mean decrease in weight of 4rd-infestation ticks which dropped from sheep fed lucerne was 26.2% compared to 16.6% for ticks from sheep which were fed on grass.Hosts maintained on a low-protein diet failed to acquire resistance to ticks, lost weight and developed anaemia while those on a high-protein diet developed resistance, maintained weight and did not develop anaemia.The nutritional stress of the hosts and its application in South Africa are discussed.     

The effect of protein content of the diet on the rate of urea formation in sheep liver

1. In the livers of six sheep given a high-protein diet, the concentrations of certain urea-cycle enzymes [ornithine transcarbamoylase, arginine synthetase (combined activity of argininosuccinate synthetase and argininosuccinase) and arginase] were significantly greater than when the sheep were given a low-protein diet. Alkaline phosphatase activity/mg. of liver protein was not significantly affected by diet. 2. Three sheep previously given the high-protein diet showed no significant rise in the concentration of ammonia in the blood after the administration of urea (0·5g./kg. body wt.). The concentration of ammonia in the blood of the three sheep given the low-protein diet rose exponentially with time after dosing with urea and all sheep died. 3. It is suggested that tolerance to ammonia toxicity in the sheep is at least partly a function of the activity of the urea-cycle enzymes in the liver.     

Getting a head start: diet, sub-adult growth, and associative learning in a seed-eating passerine

Developmental stress, and individual variation in response to it, can have important fitness consequences. Here we investigated the consequences of variable dietary protein on the duration of growth and associative learning abilities of zebra finches, Taeniopygia guttata, which are obligate graminivores. The high-protein conditions that zebra finches would experience in nature when half-ripe seed is available were mimicked by the use of egg protein to supplement mature seed, which is low in protein content. Growth rates and relative body proportions of males reared either on a low-protein diet (mature seed only) or a high-protein diet (seed plus egg) were determined from body size traits (mass, head width, and tarsus) measured at three developmental stages. Birds reared on the high-protein diet were larger in all size traits at all ages, but growth rates of size traits showed no treatment effects. Relative head size of birds reared on the two diets differed from age day 95 onward, with high-diet birds having larger heads in proportion to both tarsus length and body mass. High-diet birds mastered an associative learning task in fewer bouts than those reared on the low-protein diet. In both diet treatments, amount of sub-adult head growth varied directly, and sub-adult mass change varied inversely, with performance on the learning task. Results indicate that small differences in head growth during the sub-adult period can be associated with substantial differences in adult cognitive performance. Contrary to a previous report, we found no evidence for growth compensation among birds on the low-protein diet. These results have implications for the study of vertebrate cognition, developmental stress, and growth compensation.     

HETEROCHRONY AND ALLOMETRY: LESSONS FROM THE WATER STRIDER GENUS LIMNOPORUS

Heterochrony and allometry both deal with evolutionary modifications of ontogenies. Although data about both morphology and age are required to identify heterochronic processes, age data are not needed to study allometry. Using a simple graphical model, we show that allometric patterns cannot be used to infer the underlying heterochronic processes. We present a case study of the water strider genus Limnoporus Stål (Heteroptera: Gerridae) to illuminate the distinct roles that allometry and heterochrony play in integrated studies of the evolution of form. Multivariate analyses reveal several evolutionary modifications of growth trajectories (changes in direction, lateral transposition, and ontogenetic scaling), which are fairly consistent with the hypothesized phylogeny of the genus. Because there is no positive correlation between instar durations and size increments, size cannot be used as a proxy for age data in studies of heterochrony. In fact, a measure of overall size itself shows a remarkable variety of heterochronic changes among the six species. Mixtures of several heterochronic processes predominate over the more unitary reflections of “pure” processes. Heterochronic changes in different branches of the phylogeny, apparently independent of size scaling, suggest considerable potential for adaptive evolution. “Local” differentiation of ontogenetic traits within small clades may be at least as important as “global” evolutionary trends in large clades and will often be missed in “global” analyses.     

Time course of urinary excretion of intraportal ammonia as uric acid and ammonia in chickens fed low- or high-protein diet

15N-ammonia was intraportally infused for 6 hr into chickens fed 5% or 20% protein diet to examine the time course of urinary excretion of intraportal ammonia and dietary effects on it. Urinary ammonia increased linearly for the first hour to the same extent in both dietary groups and thereafter further in the low-protein group. Urinary uric acid derived from the intraportal ammonia adaptively increased and reached a steady state level within 1.5 hr. This level was four times higher in the high-protein group. The infused ammonia was excreted into urine as both ammonia and uric acid, in relatively high proportions in the chickens fed the low-protein diet but was almost all excreted as uric acid in those fed the high-protein diet.     

Inflorescence morphology, heterochrony, and phytogeny in the mimosoid tribes ingeae and acacieae (Leguminosae: Mimosoideae)

In earlier work (Grimes, 1992) on inflorescence morphology in the mimosoid tribes Ingeae and Acacieae I proposed that differences in inflorescence morphology result from three properties: the organization of components of the inflorescence and their relative positions; the hierarchical arrangement of the axes of the inflorescence and the position they assume in total tree architecture; and the heterochronic development of components of the inflorescence. Further work shows that the first two properties are better stated in terms of heterochrony; namely, that the organization of components of the inflorescence differs due to differences in timing of the development of organ systems and that the hierarchy of axes likewise differs due to heterochronic changes. Neither de novo origin of organs or organ systems nor suppression or loss of organs or organ systems accounts for the diversity in form. Observed heterochronic differences in the inflorescence structure may be divided into three types: spatial differences in the relationship between the unit inflorescence and the subtending leaf (hysteranthy); differences in the time of formation and/or the duration of whole axes; and changes in development pathways, leading to shoot dimorphism. These heterochronies are used as characters in a cladistic analysis, and it is shown that although some are homoplasious, many provide synapomorphies of clades of exemplars representing genera in the Ingeae and Acacieae.