The physiological basis for faster growth in the Sydney rock oyster, Saccostrea commercialis

Sydney rock oysters were sampled from a mass selection experiment for growth (the "selected" category) and from a control ("not selected") population and held in the laboratory at three ration levels. We evaluated three models to explain faster rates of growth by selected oysters. Selection resulted in oysters feeding at up to twice the rate and with greater metabolic efficiency than controls. A field experiment confirmed that selection leads to faster rates of feeding across a wide range of food concentrations. Selected oysters also grew more efficiently, at a smaller cost of growth (Cg): mean values for Cg were 0.43 J x J(-1) in selected individuals and 0.81 J x J(-1) in the controls. In contrast, oysters in both categories showed similar metabolic rates at maintenance, i.e., at a ration supporting zero growth. There was no evidence that differential energy allocation affected the balance between total metabolic requirements above and below zero net energy balance. By experimenting with selected and control oysters of different sizes and ages, then standardizing the data for size, we found no effects of age on the differences due to selection. Faster-growing oysters feed more rapidly; invest more energy per joule ingested; show a higher net growth efficiency; and are able to allocate less energy per unit of tissue growth, than slower-growing individuals.     

Physiological components of growth differences between individual oysters (Crassostrea gigas) and a comparison with Saccostrea commercialis

Pacific oysters (Crassostrea gigas) of identical age from two genetically distinct lines, one fast growing and the other slow growing, were held at three levels of ration and analysed for physiological traits to explain differences in their rates of growth. The data supported three hypotheses; faster growth was associated with faster rates of consumption of food, reduced metabolic rate at maintenance (i.e., at zero growth), and reduced metabolic costs of growth. A comparison with the Sydney rock oyster, Saccostrea commercialis, based on similar experiments on the two species, indicated that faster growth of Pacific oysters depended on similar physiological differences; the mean metabolic costs of growth, however, were similar in the two species. It is suggested that a general model for genetically linked differences in the growth rate of bivalve molluscs will need to include the processes of metabolic control rather than relying solely on an analysis of the individual components of the energetics of growth.     

Phenotypic flexibility and physiological tradeoffs in the feeding and growth of marine bivalve molluscs

Bivalve molluscs have a highly plastic feeding and growth physiology.The increasing availability of families artificially selectedfor faster growth has enabled physiological experiments to investigatethe genetic basis for variable rates of growth. Fast growthis achieved by a combination of increased rates of feeding,reduced metabolic rates and lower metabolic costs of growth.In at least one species there is a trade-off between growthin protein and the storage of lipids that are utilized in gametogenesis.Energy requirements for maintenance are also higher in slow-growingindividuals. Reduced costs of growth are due in part to increasedefficiencies of protein turnover. Nevertheless, high proteinturnover (and therefore high metabolic cost) may benefit fitnessin the later stages of gametogenesis. Faster feeding rates donot impair flexibility in feeding behavior which compensatesfor changes in the food environment. Both inter- and intra-speciesdifferences in feeding behavior are evident and suggest possibleconstraints imposed by faster feeding on the efficiency of selectionbetween food particles of different nutritional value.     

Multiple-Locus Heterozygosity and the Physiological Energetics of Growth in the Coot Clam, MULINIA LATERALIS, from a Natural Population

The relationship between individual energy budgets and multiple-locus heterozygosity at six polymorphic enzyme loci was examined in Mulinia lateralis. Energy budgets were determined by measuring growth rates, rates of oxygen consumption, ammonia excretion and clearance rates. Enzyme genotypes were determined using starch gel electrophoresis. Growth rate and net growth efficiency (the ratio of energy available for growth to total energy absorbed) increased with individual heterozygosity. The positive relationship between observed growth and multiple-locus heterozygosity was associated with a negative relationship between routine metabolic costs and increasing heterozygosity. Reduction in routine metabolic costs explained 60% of the observed increased growth of more heterozygous individuals. When routine metabolic costs were standardized for differences in feeding rates, these standard metabolic costs explained 97% of the differences in growth rate. Lower standard metabolic costs, associated with increasing heterozygosity, have been proposed as a physiological mechanism for the relationship between multiple-locus heterozygosity and growth rate that has been reported for a variety of organisms, ranging in diversity from aspens to humans. This study demonstrates that reduction of standard metabolic costs, at least in clams, accounts for virtually all of the differences in growth rate among individuals of differing heterozygosity.     

Direct effects of physical stress can be counteracted by indirect benefits: oyster growth on a tidal elevation gradient

The paradigmatic gradient for intertidal marine organisms of increasing physical stress from low to high elevation has long served as the basis for using direct effects of duration of water coverage to predict many biological patterns. Accordingly, changes in potential feeding time may predict the direction and magnitude of differences between elevations in individual growth rates of sessile marine invertebrates. Oysters (triploid Crassostrea ariakensis) experimentally introduced at intertidal (MLW+0.05 m) and subtidal (MLW–0.25 m) elevations in racks provided a test of the ability to use duration of water coverage to predict changes in growth. During early-to-mid winter, a depression of 38–47% in shell growth of intertidal oysters matched the 36% reduction in available feeding time relative to subtidal oysters. In late winter as solar heating of exposed oysters increased, growth differences of 52–55% departed only slightly from the predicted 39%. In spring, however, duration of water coverage failed to predict even the correct direction of growth change with elevation as intertidal oysters grew 34% faster despite 39% less feeding time. Intense seasonal development of shell fouling by other suspension feeders like ascidians, mussels, and barnacles on subtidal (94% incidence) but not on aerially exposed intertidal (21–38% incidence) oysters may explain why duration of water cover failed to predict spring growth differences. Less intense fouling develops on intertidal oysters due to the physiological stress of aerial exposure on settlers, especially during higher temperatures and longer solar exposures of spring. Fouling by suspension feeders is known to reduce growth of the host through localized competition for food and added energetic costs. Thus, in springtime, indirect effects of aerial exposure providing a partial refuge from biological enemies overwhelmed direct effects of reduced duration of water coverage to reverse the expected pattern of slower intertidal growth of a marine invertebrate.     

Elevational variation in adult body size and growth rate but not in metabolic rate in the tree weta Hemideina crassidens

Populations of the same species inhabiting distinct localities experience different ecological and climatic pressures that might result in differentiation in traits, particularly those related to temperature. We compared metabolic rate (and its thermal sensitivity), growth rate, and body size among nine high- and low-elevation populations of the Wellington tree weta, Hemideina crassidens, distributed from 9 to 1171 m a.s.l across New Zealand. Our results did not indicate elevational compensation in metabolic rates (metabolic cold adaptation). Cold acclimation decreased metabolic rate compared to warm-acclimated individuals from both high- and low-elevation populations. However, we did find countergradient variation in growth rates, with individuals from high-elevation populations growing faster and to a larger final size than individuals from low-elevation populations. Females grew faster to a larger size than males, although as adults their metabolic rates did not differ significantly. The combined physiological and morphological data suggest that high-elevation individuals grow quickly and achieve larger size while maintaining metabolic rates at levels not significantly different from low-elevation individuals. Thus, morphological differentiation among tree weta populations, in concert with genetic variation, might provide the material required for adaptation to changing conditions.     

Rapid growth reduces cold resistance: evidence from latitudinal variation in growth rate, cold resistance and stress proteins

Background

Physiological costs of rapid growth may contribute to the observation that organisms typically grow at submaximal rates. Although, it has been hypothesized that faster growing individuals would do worse in dealing with suboptimal temperatures, this type of cost has never been explored empirically. Furthermore, the mechanistic basis of the physiological costs of rapid growth is largely unexplored.

Methodology/Principal Finding

Larvae of the damselfly Ischnura elegans from two univoltine northern and two multivoltine southern populations were reared at three temperatures and after emergence given a cold shock. Cold resistance, measured by chill coma recovery times in the adult stage, was lower in the southern populations. The faster larval growth rates in the southern populations contributed to this latitudinal pattern in cold resistance. In accordance with their assumed role in cold resistance, Hsp70 levels were lower in the southern populations, and faster growing larvae had lower Hsp70 levels. Yet, individual variation in Hsp70 levels did not explain variation in cold resistance.

Conclusions/Significance

We provide evidence for a novel cost of rapid growth: reduced cold resistance. Our results indicate that the reduced cold resistance in southern populations of animals that change voltinism along the latitudinal gradient may not entirely be explained by thermal selection per se but also by the costs of time constraint-induced higher growth rates. This also illustrates that stressors imposed in the larval stage may carry over and shape fitness in the adult stage and highlights the importance of physiological costs in the evolution of life-histories at macro-scales.     

Many QTLs with minor additive effects are associated with a large difference in growth between two selection lines in chickens

Two growth-selected lines in chickens have been developed from a single founder population by divergent selection for body weight at 56 days of age. After more than 40 generations of selection they show a nine-fold difference in body weight at selection age and large differences in growth rate, appetite, fat deposition and metabolic characteristics. We have generated a large intercross between these lines comprising more than 800 F2 birds. QTL mapping revealed 13 loci affecting growth. The most striking observation was that the allele in the high weight line in all cases was associated with enhanced growth, but each locus explained only a small proportion of the phenotypic variance using a standard QTL model (1.3-3.1%). This result is in sharp contrast to our previous study where we reported that the two-fold difference in adult body size between the red junglefowl and White Leghorn domestic chickens is explained by a small number of QTLs with large additive effects. Furthermore, no QTLs for anorexia or antibody response were detected despite large differences for these traits between the founder lines. The result is an excellent example where a large phenotypic difference between populations occurs in the apparent absence of any single locus with large phenotypic effects. The study underscores the need for powerful experimental designs in genetic studies of multifactorial traits. No QTL at all would have reached genome-wide significance using a less powerful design (e.g. approx. 200 F2 individuals) regardless of the nine-fold phenotypic difference between the founder lines for the selected trait.     

Coevolution of color pattern and thermoregulatory behavior in polymorphic pygmy grasshoppers Tetrix undulata

Ectothermic organisms, such as insects and reptiles, rely on external heat sources to control body temperature and possess physiological and behavioral traits that are temperature dependent. It has therefore been hypothesised that differences in body temperature resulting from phenotypic properties, such as color pattern, may translate into selection against thermally inferior phenotypes. We tested for costs and benefits of pale versus dark coloration by comparing the behaviors (i.e., basking duration and bouts) of pygmy grasshopper (Tetrix undulata) individuals exposed to experimental situations imposing a trade-off between temperature regulation and feeding. We used pairs consisting of two full-siblings of the same sex that represented different (genetically coded) color morphs but had shared identical conditions from the time of fertilization. Our results revealed significant differences in behavioral thermoregulation between dark and pale individuals in females, but not in males. Pale females spent more time feeding than dark females, regardless of whether feeding was associated with a risk of either hypothermia or overheating. In contrast, only minor differences in behavior (if any) were evident between individuals that belonged to the same color morph but had been painted black or gray to increase and decrease their heating rates. This suggests that the behavioral differences between individuals belonging to different color morphs are genetically determined, rather than simply reflecting a response to different heating rates. To test for effects of acclimation on behaviors, we used pairs of individuals that had been reared from hatchlings to adults under controlled conditions in either low or high temperature. The thermal regime experienced during rearing had little effect on behaviors during the experiments reported above, but significantly influenced the body temperatures selected in a laboratory thermal gradient. In females (but not in males) preferred body temperature also varied among individuals born to mothers belonging to different color morphs, suggesting that a genetic correlation exists between color pattern and temperature preferences. Collectively, these findings, at least in females, are consistent with the hypothesis of multiple-trait coevolution and suggest that the different color morphs represent alternative evolutionary strategies.     

Carbon and nitrogen relationships in the feeding and growth of the Pacific oyster, Crassostrea gigas (Thunberg)

Bivalve molluscs, in common with consumers in general, use behavioral and physiological mechanisms to balance metabolic requirements with available nutrients. This study considered how the Pacific oyster, Crassostrea gigas, meets the demands of growth and maintenance, measured in terms of carbon and nitrogen, in a variable food environment. Stoichiometry theory helped to evaluate: a) whether feeding behaviour modifies the intake of C and N given seasonal variability in food quality: b) how rates of metabolism and excretion, and C and N growth efficiencies, respond to mismatch between nutrient intake and the oysters' needs. Two field experiments in the Port Stephens estuary, near Sydney, Australia, measured feeding behaviour, metabolic and growth rates relative to seasonal changes in food supply. In a laboratory experiment, relationships between physiological rates and growth were measured to test a model of growth as a function of absorption of C and N. Potential metabolic targets for compensation were the C/N ratios of body tissues, maintenance and/or of soft tissue added as growth. C/N of whole soft issues varied little during the year (mean 5.4). In July (a time of low food availability of poor quality) growth was negligible and the C/N (maintenance) target was 6.7. In March (abundant food of high quality) growth was rapid with a high N-demand; the C/N of growth was 3.9. In November (medium food quality) there was an enhanced C-demand for glycogen storage; the C/N of growth was 7.9. Feeding behaviour changed the balance between C and N intake across months, primarily due to changes in the selection efficiency for nitrogen, which was highest at low filtration rates on particles of high C/N ratio. Nitrogen intake was favoured over C in July. In November, C-intake increased relative to N. In March, when abundant food nitrogen coincided with a high demand for growth, feeding behaviour was neutral with respect to C/N ratios. In all cases C/N of absorbed matter was greater than the C/N of growth. Growth efficiencies for carbon declined with increased C/N of ingested matter due to higher metabolic increments (SDA) when feeding on lower food quality; the metabolic costs of growth did not vary. In contrast, growth efficiencies for nitrogen did not alter with C/N for ingested matter, due in part to increased nitrogen losses, relative to tissue nitrogen content, when feeding on low C/N food. Nitrogen was therefore conserved metabolically relative to C. Both feeding and metabolic processes contributed to compensation for the mismatch between seasonally variable food quality and the demands of growth.     

The potential for disruptive selection on growth rates across genetically influenced alternative reproductive tactics

A trade-off between survival to sexual maturity and mating success is common across alternative reproductive tactics (ARTs), and can lead to tactical disruptive selection on shared traits (i.e. positive selection gradient in one tactic, and negative selection gradient in another). We were interested in examining the theoretical possibility of tactical disruptive selection on intrinsic growth rate. The male ARTs in Xiphophorus multilineatus express two distinct life histories: “courters” optimize mating success by maturing later at larger size and coaxing females to mate, while “sneakers” optimize survival to sexual maturity by maturing earlier at a smaller size, using both coaxing and coercive mating behaviors. In addition to differences in mating behaviors, body length, body depth, and the pigment pattern vertical bars, courter males grow faster than sneaker males. We present a new hypothesis for differences in growth rates between genetically influenced ARTs. The “growth-maturity optimization” hypothesis suggests that ARTs with differences in the probability of surviving to sexual maturity may have different optimal growth rates, leading to tactical disruptive selection. We also present a simple model to suggest that when considering both a cost and benefit to faster growth, tactical disruptive selection on growth rates is theoretically possible. In our model, the value that determines when tactical disruptive selection on growth rate will occur is the increase in probability of survival to sexual maturity gained through faster growth multiplied by the cost of faster growth (reduced longevity). Finally, we present empirical evidence to support the prediction that faster growth has a cost in X. multilineatus: in a controlled laboratory setting, courter males that did not survive 1.2 years past sexual maturity grew faster as juveniles (14–70 days) than those that survived.     

The evolution of sexual size dimorphism in the house finch. III. Developmental basis

Sexual size dimorphism of adults proximately results from a combination of sexually dimorphic growth patterns and selection on growing individuals. Yet, most studies of the evolution of dimorphism have focused on correlates of only adult morphologies. Here we examined the ontogeny of sexual size dimorphism in an isolated population of the house finch (Carpodacus mexicanus). Sexes differed in growth rates and growth duration; in most traits, females grew faster than males, but males grew for a longer period. Sexual dimorphism in bill traits (bill length, width, depth) and in body traits (wing, tarsus, and tail length; mass) developed during different periods of ontogeny. Growth of bill traits was most different between sexes during the juvenile period (after leaving the nest), whereas growth of body traits was most sexually dimorphic during the first few days after hatching. Postgrowth selection on juveniles strongly influenced sexual dimorphism in all traits; in some traits, this selection canceled or reversed dimorphism patterns produced by growth differences between sexes. The net result was that adult sexual dimorphism, to a large degree, was an outcome of selection for survival during juvenile stages. We suggest that previously documented fast and extensive divergence of house finch populations in sexual size dimorphism may be partially produced by distinct environmental conditions during growth in these populations.     

The effect of brain size evolution on feeding propensity,digestive efficiency,and juvenile growth

One key hypothesis in the study of brain size evolution is the expensive tissue hypothesis; the idea that increased investment into the brain should be compensated by decreased investment into other costly organs, for instance the gut. Although the hypothesis is supported by both comparative and experimental evidence, little is known about the potential changes in energetic requirements or digestive traits following such evolutionary shifts in brain and gut size. Organisms may meet the greater metabolic requirements of larger brains despite smaller guts via increased food intake or better digestion. But increased investment in the brain may also hamper somatic growth. To test these hypotheses we here used guppy (Poecilia reticulata) brain size selection lines with a pronounced negative association between brain and gut size and investigated feeding propensity, digestive efficiency (DE), and juvenile growth rate. We did not find any difference in feeding propensity or DE between large‐ and small‐brained individuals. Instead, we found that large‐brained females had slower growth during the first 10 weeks after birth. Our study provides experimental support that investment into larger brains at the expense of gut tissue carries costs that are not necessarily compensated by a more efficient digestive system.     

Faster development does not lead to correlated evolution of greater pre-adult competitive ability in Drosophila melanogaster

In comparisons across Drosophila species, faster pre-adult development is phenotypically correlated with increased pre-adult competitive ability, suggesting that these two traits may also be evolutionary correlates of one another. However, correlations between traits within- and among- species can differ, and in most cases it is the within-species genetic correlations that are likely to act as constraints on adaptive evolution. Moreover, laboratory studies on Drosophila melanogaster have shown that the suite of traits that evolves in populations subjected to selection for faster development is the opposite of the traits that evolve in populations selected for increased pre-adult competitive ability. This observation led us to propose that, despite having a higher carrying capacity and a reduced minimum food requirement for completing development than controls, D. melanogaster populations subjected to selection for faster development should have lower competitive ability than controls owing to their reduced larval feeding rates and urea tolerance. Here, we describe results from pre-adult competition experiments that clearly show that the faster developing populations are substantially poorer competitors than controls when reared at high density in competition with a marked mutant strain. We briefly discuss these results in the context of different formulations of density-dependent selection theory.     

Correlated responses to selection for faster development and early reproduction in Drosophila: the evolution of larval traits

Studies on selection for faster development in Drosophila have typically focused on the trade-offs among development time, adult weight, and adult life span. Relatively less attention has been paid to the evolution of preadult life stages and behaviors in response to such selection. We have earlier reported that four laboratory populations of D. melanogaster selected for faster development and early reproduction, relative to control populations, showed considerably reduced preadult development time and survivorship, dry weight at eclosion, and larval growth rates. Here we study the larval phase of these populations in greater detail. We show here that the reduction in development time after about 50 generations of selection is due to reduced duration of the first and third larval instars and the pupal stage, whereas the duration of the second larval instar has not changed. About 90% of the preadult mortality in the selected populations is due to larval mortality. The third instar larvae, pupae, and freshly eclosed adults of the selected populations weigh significantly less than controls, and this difference appears during the third larval instar. Thereafter, percentage weight loss during the pupal stage does not differ between selected and control populations. The minimum amount of time a larva must feed to subsequently complete development is lower in the selected populations, which also exhibit a syndrome of reduced energy expenditure through reduction in larval feeding rate, larval digging and foraging activity, and pupation height. Comparison of these results with those observed earlier in populations selected for adaptation to larval crowding and faster development under a different protocol from ours reveal differences in the evolved traits that suggest that the responses to selection for faster development are greatly affected by the larval density at which selection acts and on details of the selection pressures acting on the timing of reproduction.     

How to become large quickly: quantitative genetics of growth and foraging in a flush feeding lepidopteran larva

Rapid larval growth in insects may be selected for by rapid ephemeral phenological changes in food resources modifying the structure of phenotypic and genetic (co)variation in and among individual traits. We studied the relative effects of three processes which can modify expression of additive genetic and nongenetic variation in traits. First, natural selection tends to erode genetic variation in fitness-related traits. Second, there may be high variance even in traits closely coupled with fitness, if these traits are themselves products of variable lower level traits. Third, traits may be canalized by developmental processes which reduce phenotypic variation. Moreover, we investigated the phenotypic and genetic role played by the underlying traits in attaining simultaneously both large size and short development time. We measured phenotypic and genetic (co)variation in several pre- and post-ingestive foraging traits, growth, development rate, development time and size, together forming a hierarchical network of traits, in the larvae of a flush feeding geometrid, Epirrita autumnata. Rapid larval growth rate and high pupal mass are closely related to fitness in E. autumnata. Traits closely associated with larval growth displayed low levels of additive genetic variation, indicating that genetic variability may have been exhausted by selection for rapid growth. The body size of E. autumnata, in spite of its close correlation with fitness, exhibited a significant additive genetic variation, possiblye because caterpillar size is the outcome of many underlying heritable traits. The low level traits in the hierarchical net, number (indicating larval movements) and size of feeding bouts in leaves, relative consumption rate and efficiency of conversion of ingested food, displayed high levels of residual variation. High residual variation in consumption and physiological ability to handle leaf material resulted from their flexibility which reduced variation in growth rate, i.e. growth rate was canalized. We did not detect a trade-off between development time and final size. On the contrary, large pupal masses were attained by short larval periods, and this relationship was strongly genetically determined, suggesting that both developmental time and final size are expressions of the same developmental process (vigorous growth) and the same genes (or linkage disequilibrium).     

Individuals Maintain Similar Rates of Protein Synthesis over Time on the Same Plane of Nutrition under Controlled Environmental Conditions

Consistent individual differences in animal performance drive individual fitness under variable environmental conditions and provide the framework through which natural selection can operate. Underlying this concept is the assumption that individuals will display consistent levels of performance in fitness-related traits and interest has focused on individual variation and broad sense repeatability in a range of behavioural and physiological traits. Despite playing a central role in maintenance and growth, and with considerable inter-individual variation documented, broad sense repeatability in rates of protein synthesis has not been assessed. In this study we show for the first time that juvenile flounder Platichthys flesus reared under controlled environmental conditions on the same plane of nutrition for 46 days maintain consistent whole-animal absolute rates of protein synthesis (A_s). By feeding meals containing ¹⁵N-labelled protein and using a stochastic end-point model, two non-terminal measures of protein synthesis were made 32 days apart (d₁₄ and d₄₆). A_s values (mass-corrected to a standard mass of 12 g) showed 2- to 3-fold variation between individuals on d₁₄ and d₄₆ but individuals showed similar A_s values on both days with a broad sense repeatability estimate of 0.684 indicating significant consistency in physiological performance under controlled experimental conditions. The use of non-terminal methodologies in studies of animal ecophysiology to make repeat measures of physiological performance enables known individuals to be tracked across changing conditions. Adopting this approach, repeat measures of protein synthesis under controlled conditions will allow individual ontogenetic changes in protein metabolism to be assessed to better understand the ageing process and to determine individual physiological adaptive capacity, and associated energetic costs of adaptation, to global environmental change.     

Seasonal variability in feeding behaviour, metabolic rates and carbon and nitrogen balances in the Sydney oyster, Saccostrea glomerata (Gould)

To establish if nutrients limit the growth of bivalves requires information not only on the quality of food available, but also the animals' feeding behaviour and endogenous metabolic demands. We hypothesized that growth of the Sydney rock oyster (Saccostrea glomerata) would vary in response to seasonal changes in food quality rather than quantity. We also predicted that the oysters would show feeding preferences for nitrogen over carbon, and this behaviour would result in carbon/nitrogen (C/N) ratios for ingested and absorbed matter that would be lower than the C/N of both the seston and the oysters' estimated metabolic maintenance requirements. The experiments were done in two phases under natural conditions. In phase 1, feeding behaviour was assessed on a single occasion and the results used to pose hypotheses for testing in phase 2, which included measurements made on three occasions encompassing autumn, winter and spring conditions. Growth rates varied with changes in ambient food quality and not with the concentration of total suspended matter. Feeding behaviour responded to food quality and, in most cases, resulted in nitrogen enrichment. For example, when nitrogen was potentially limiting to growth and/or maintenance, due to high food C/N (July) or high nitrogen demand (March), pre-ingestive selection ensured nitrogen enrichment of ingested matter and C/N ratios of ingested matter which were below the maintenance requirement. However, in November, when endogenous demands indicated an increased requirement for carbon, feeding behaviour resulted in carbon enrichment, an increase in carbon conversion efficiency, and ingested C/N ratios greater than the maintenance requirement. The results support the assertion of variable feeding physiology in oysters, responsive to both exogenous (seasonal differences in carbon and nitrogen availability) and endogenous (cycles of reproduction and growth) factors.