Biphasic growth in fish II: empirical assessment

In [Quince, et al., 2008. Biphasic growth in fish I: Theoretical foundations. J. Theor. Biol., doi:10.1016/j.jtbi.2008.05.029], we developed a set of biphasic somatic growth models, where maturation is accompanied by a deceleration of growth due to allocation of energy to reproduction. Here, we use growth data from both hatchery-raised and wild populations of a large freshwater fish (lake trout, Salvelinus namaycush) to test these models. We show that a generic biphasic model provides a better fit to these data than the von Bertalanffy model. We show that the observed deceleration of somatic growth in females varies directly with gonad weight at spawning, with observed egg volumes roughly 50% of the egg volumes predicted under the unrealistic assumption of perfectly efficient energy transfer from somatic lipids to egg lipids. We develop a Bayesian procedure to jointly fit a biphasic model to observed growth and maturity data. We show that two variants of the generic biphasic model, both of which assume that annual allocation to reproduction is adjusted to maximise lifetime reproductive output, provide complementary fits to wild population data: maturation time and early adult growth are best described by a model with no constraints on annual reproductive investment, while the growth of older fish is best described by a model that is constrained so that the ratio of gonad size to somatic weight (g) is fixed. This behaviour is consistent with the additional observation that g increases with size and age among younger, smaller breeding females but reaches a plateau among older, larger females. We then fit both of these optimal models to growth and maturation data from nineteen wild populations to generate population-specific estimates of ‘adapted mortality’ rate: the adult mortality consistent with observed growth and maturation schedules, given that both schedules are adapted to maximise lifetime reproductive output. We show that these estimates are strongly correlated with independent estimates of the adult mortality experienced by these populations.     

A Cell-based Model of Endothelial Cell Migration,Proliferation and Maturation During Corneal Angiogenesis

The motivation of this work stems from two critical experimental observations associated with corneal angiogenesis: (1) angiogenesis will not succeed without endothelial cell proliferation, and (2) proliferation mainly occurs at the leading edge of developing sprouts (Sholley et al., Lab. Invest. 51:624–634, 1984). To discover the underlying mechanisms of these phenomena, we develop a cell-based mathematical model that integrates a mechanical model of elongation with a biochemical model of cell phenotype variation regulated by angiopoietins within a developing sprout. This model allows for a detailed study of the relative roles of endothelial cell migration, proliferation, and maturation. The model is validated by quantitatively comparing its predictions with data derived from corneal angiogenesis experiments. We conclude that cell elasticity and cell-to-cell adhesion allow only limited sprout extension in the absence of proliferation, and the maturation process combined with bioavailability of VEGF can explain the localization of proliferation to the leading edge. We also use this model to investigate the effects of X-ray irradiation, Ang-2 inhibition, and extracellular matrix anisotropy on sprout morphology and extension.     

Lacker's model: control of follicular growth and ovulation in domestic species

Lacker (1981) and Lacker & Akin (1988) developed a mathematical model of follicular maturation and ovulation; this model of only four parameters accounts for a large number of results obtained over the past decade or more on the control of follicular growth and ovulation in mammals. It establishes a single law of maturation for each follicle which describes the interactions between growing follicles. The function put forward is sufficient to explain the constancy of the number of ovulations or large follicles in a female as well as the variability of this number among strains or species and for either induced or spontaneous ovulators. According to the model, the number of ovulations or large follicles lies between two limits that are themselves simple functions of two parameters of the model. Moreover, Lacker's model exhibits interesting characteristics in agreement with results obtained by physiologists: in particular, it predicts that the number of ovulating or large follicles is independent of:

1. the total number of maturing follicles,
2. the process of recruitment of newly maturing follicles towards the terminal maturation (Poisson or other),
3. the form of the LH or FSH secretion curves as functions of the systemic level of oestradiol. The model further predicts that
4. selection and dominance of follicles result from the feedback between the ovary and the hypophysis through the interactions between follicles; these interactions are expressed by the maturation function of the model.
5. recovery from atresia is possible for a follicle: from decreasing, the rate of secretion of oestradiol may increase.
6. the revised model suggests a renewal of follicles during the sexual cycle, as “waves of follicular growth”.

Lacker's model is a model of strict dominance; it maintains a hierarchy of the follicles as soon as they start their final maturation to the ovulations as that is observed in bird or reptile ovary. Such a strict hierarchy is possible but it is probably not a general situation in all mammals. We therefore modified the maturing function of the follicle in order to make it compatible with the observations of physiologists: follicles always interact as in the initial model but they individually become old, the hierarchy of follicles can be modified with time and the largest follicles do not indefinitely grow as in the initial model.     

Persistent host–parasitoid interaction caused by host maturation variability

The heterogeneity of parasitism risk among host individuals is a key factor for stabilizing or sustaining host–parasitoid interactions. Host maturation variability, or the variation in the maturation times among host individuals, is the simplest source of such heterogeneity, but it has often been neglected in previous theoretical studies. We developed a configuration individual-based model (cIBM) of host–parasitoid interaction to investigate to what degree of host maturation variability promotes the persistence of host–parasitoid interactions. We ran simulations with various degrees of host maturation variability for different lengths of unsusceptible period. The result showed that low host maturation variability could sustain host–parasitoid dynamics when the host-unsusceptible period was short. Conversely, high levels of variability could sustain host–parasitoid dynamics when the host-unsusceptible period was about half of the total larval period. This suggests that the balance between variability and unsusceptible period is important for the persistence of host–parasitoid interaction. We conclude that maturation variability is a factor that can contribute to the sustainment of host–parasitoid interactions.     

Autophagy proteins are not universally required for phagosome maturation

Phagocytosis plays a central role in immunity and tissue homeostasis. After internalization of cargo into single-membrane phagosomes, these compartments undergo a maturation sequences that terminates in lysosome fusion and cargo degradation. Components of the autophagy pathway have recently been linked to phagosome maturation in a process called LC3-associated phagocytosis (LAP). In this process, autophagy machinery is thought to conjugate LC3 directly onto the phagosomal membrane to promote lysosome fusion. However, a recent study has suggested that ATG proteins may in fact impair phagosome maturation to promote antigen presentation. Here, we examined the impact of ATG proteins on phagosome maturation in murine cells using FCGR2A/FcγR-dependent phagocytosis as a model. We show that phagosome maturation is not affected in Atg5-deficient mouse embryonic fibroblasts, or in Atg5- or Atg7-deficient bone marrow-derived macrophages using standard assays of phagosome maturation. We propose that ATG proteins may be required for phagosome maturation under some conditions, but are not universally required for this process.     

Interacting forces of predation and fishing affect species’ maturation size

1. Fishing is a strong selective force and is supposed to select for earlier maturation at smaller body size. However, the extent to which fishing‐induced evolution is shaping ecosystems remains debated. This is in part because it is challenging to disentangle fishing from other selective forces (e.g., size‐structured predation and cannibalism) in complex ecosystems undergoing rapid change.
2. Changes in maturation size from fishing and predation have previously been explored with multi‐species physiologically structured models but assumed separation of ecological and evolutionary timescales. To assess the eco‐evolutionary impact of fishing and predation at the same timescale, we developed a stochastic physiologically size‐structured food‐web model, where new phenotypes are introduced randomly through time enabling dynamic simulation of species'' relative maturation sizes under different types of selection pressures.
3. Using the model, we carried out a fully factorial in silico experiment to assess how maturation size would change in the absence and presence of both fishing and predation (including cannibalism). We carried out ten replicate stochastic simulations exposed to all combinations of fishing and predation in a model community of nine interacting fish species ranging in their maximum sizes from 10 g to 100 kg. We visualized and statistically analyzed the results using linear models.
4. The effects of fishing on maturation size depended on whether or not predation was enabled and differed substantially across species. Fishing consistently reduced the maturation sizes of two largest species whether or not predation was enabled and this decrease was seen even at low fishing intensities (F = 0.2 per year). In contrast, the maturation sizes of the three smallest species evolved to become smaller through time but this happened regardless of the levels of predation or fishing. For the four medium‐size species, the effect of fishing was highly variable with more species showing significant and larger fishing effects in the presence of predation.
5. Ultimately our results suggest that the interactive effects of predation and fishing can have marked effects on species'' maturation sizes, but that, at least for the largest species, predation does not counterbalance the evolutionary effect of fishing. Our model also produced relative maturation sizes that are broadly consistent with empirical estimates for many fish species.

     

Two zinc finger proteins, OMA-1 and OMA-2, are redundantly required for oocyte maturation in C. elegans.

Oocytes are released from meiotic prophase I arrest through a process termed oocyte maturation. We present here a genetic characterization of oocyte maturation, using C. elegans as a model system. We show that two TIS11 zinc finger-containing proteins, OMA-1 and OMA-2, express specifically in maturing oocytes and function redundantly in oocyte maturation. Oocytes in oma-1;oma-2 mutants initiate but do not complete maturation and arrest at a defined point in prophase I. Two maturation signal-induced molecular events, including the maintenance of activated MAP kinase, do not occur in Oma oocytes. The Oma prophase arrest is released by inactivation of a MYT-1-like kinase, suggesting that OMA-1 and OMA-2 function upstream of MYT-1 as positive regulators of prophase progression during meiotic maturation.     

Food web framework for size-structured populations

We synthesise traditional unstructured food webs, allometric body size scaling, trait-based modelling, and physiologically structured modelling to provide a novel and ecologically relevant tool for size-structured food webs. The framework allows food web models to include ontogenetic growth and life-history omnivory at the individual level by resolving the population structure of each species as a size-spectrum. Each species is characterised by the trait ‘size at maturation’, and all model parameters are made species independent through scaling with individual body size and size at maturation. Parameter values are determined from cross-species analysis of fish communities as life-history omnivory is widespread in aquatic systems, but may be reparameterised for other systems. An ensemble of food webs is generated and the resulting communities are analysed at four levels of organisation: community level, species level, trait level, and individual level. The model may be solved analytically by assuming that the community spectrum follows a power law. The analytical solution provides a baseline expectation of the results of complex food web simulations, and agrees well with the predictions of the full model on biomass distribution as a function of individual size, biomass distribution as a function of size at maturation, and relation between predator-prey mass ratio of preferred and eaten food. The full model additionally predicts the diversity distribution as a function of size at maturation.     

Synchrony of bone marrow proliferation and maturation as the origin of cyclic haemopoiesis

Abstract. Cyclic haemopoiesis in Grey Collie dogs is characterized by stable oscillations in all haemopoietic lineages. It is proposed that in these animals, in contrast to normal animals, the maturation process of haemopoietic (in particular granuloid) cells from the primitive progenitors to the functional cells is characterized by an abnormally strong synchrony. It is conjectured that the marrow maturation time has a very small variance compared with non-cyclic normal dogs. With a mathematical model of haemopoiesis it is shown that small fluctuations are amplified via regular feedback processes such that stable granuloid oscillations are established. Erythroid oscillations are induced indirectly by granuloid feedback to the stem cell pool. The model calculations further show that the synchrony hypothesis of bone marrow maturation can quantitatively explain the following experimental results: (1) the maintenance of stable cycles of granuloid and erythroid bone marrow and blood cells with a period of approximately 14 d; (2) the disappearance of granuloid and erythroid cycles during the administration of the colony stimulating factor rhG-CSF; (3) the reappearance of oscillations when the administration of CSF is discontinued; (4) the cessation of cycles during endotoxin application; and (5) the persistence of cycles during erythroid manipulations (bleeding anaemia, hypoxia, hypertransfusion). We therefore conclude that cyclic haemopoiesis is not caused by a defect in the regulatory control system but by an unusual maturation process.     

Synchrony of bone marrow proliferation and maturation as the origin of cyclic haemopoiesis.

Cyclic haemopoiesis in Grey Collie dogs is characterized by stable oscillations in all haemopoietic lineages. It is proposed that in these animals, in contrast to normal animals, the maturation process of haemopoietic (in particular granuloid) cells from the primitive progenitors to the functional cells is characterized by an abnormally strong synchrony. It is conjectured that the marrow maturation time has a very small variance compared with non-cyclic normal dogs. With a mathematical model of haemopoiesis it is shown that small fluctuations are amplified via regular feedback processes such that stable granuloid oscillations are established. Erythroid oscillations are induced indirectly by granuloid feedback to the stem cell pool. The model calculations further show that the synchrony hypothesis of bone marrow maturation can quantitatively explain the following experimental results: (1) the maintenance of stable cycles of granuloid and erythroid bone marrow and blood cells with a period of approximately 14 d; (2) the disappearance of granuloid and erythroid cycles during the administration of the colony stimulating factor rhG-CSF; (3) the reappearance of oscillations when the administration of CSF is discontinued; (4) the cessation of cycles during endotoxin application; and (5) the persistence of cycles during erythroid manipulations (bleeding anaemia, hypoxia, hypertransfusion). We therefore conclude that cyclic haemopoiesis is not caused by a defect in the regulatory control system but by an unusual maturation process.     

The impact of maturation delay of mosquitoes on the transmission of West Nile virus

We formulate and analyze a delay differential equation model for the transmission of West Nile virus between vector mosquitoes and avian hosts that incorporates maturation delay for mosquitoes. The maturation time from eggs to adult mosquitoes is sensitive to weather conditions, in particular the temperature, and the model allows us to investigate the impact of this maturation time on transmission dynamics of the virus among mosquitoes and birds. Numerical results of the model show that a combination of the maturation time and the vertical transmission of the virus in mosquitoes has substantial influence on the abundance and number of infection peaks of the infectious mosquitoes.     

Harvest-induced maturation evolution under different life-history trade-offs and harvesting regimes

The potential of harvesting to induce adaptive changes in exploited populations is now increasingly recognized. While early studies predicted that elevated mortalities among larger individuals select for reduced maturation size, recent theoretical studies have shown conditions under which other, more complex evolutionary responses to size-selective mortality are expected. These new predictions are based on the assumption that, owing to the trade-off between growth and reproduction, early maturation implies reduced growth. Here we extend these findings by analyzing a model of a harvested size-structured population in continuous time, and by systematically exploring maturation evolution under all three traditionally acknowledged costs of early maturation: reduced fecundity, reduced growth, and/or increased natural mortality. We further extend this analysis to the two main types of harvest selectivity, with an individual's chance of getting harvested depending on its size and/or maturity stage. Surprisingly, we find that harvesting mature individuals not only favors late maturation when the costs of early maturation are low, but promotes early maturation when the costs of early maturation are high. To our knowledge, this study therefore is the first to show that harvesting mature individuals can induce early maturation.     

Effect of prostaglandin E2, lipopolysaccharide, IFN-gamma and cytokines on the generation and function of fast-DC

BACKGROUND: Recent reports have described a new strategy for differentiation and maturation of monocyte-derived DC within only 48 h of in vitro culture (fast-DC). We compared the ability of various maturation stimuli with the generation of Ag-specific T-cell responses and generation of functional fast-DC. METHODS: CD14+ cells were treated with GM-CSF and IL-4 for 1 day to generate immature DC, and were then matured with either inflammatory cytokines or a combination of lipopolysaccharide (LPS) and INF-gamma. Mature DC were then used to study the effect of prostaglandin E2 (PGE2) on the stimulatory function of fast-DC. RESULTS: fast-DC were CD14- and expressed mature DC surface markers, and maintained this phenotype after withdrawing the cytokine from culture. Treatment of fast-DC with a combination of LPS and INF-gamma promoted the maturation of highly uniform fast-DC. The T-cell proliferative response to DC was enhanced by inclusion of PGE2 in the MCM-mimic (TNF-a, IL-1 a, IL-6, PGE2) cocktail. DISCUSSION: fast-DC are very effective; they not only reduce the labor, cost and time required for in vitro DC development, but may also represent a model more closely resembling DC differentiation from monocytes in vivo.     

A cytokinetic model for heterogeneous mammalian cell populations. I. Cell growth and cell death

A general model is proposed for describing the growth behavior of mammalian cell populations, which features:(a) a cell cycle time distribution function with properties such that mean and variance increase with increasing population size; (b) maturation age and maturation rate functions which constrain the maturational pathways of individual cells; and (c) a death rate function, where cell death is construed as irreparable damage to a cell's reproductive apparatus. The biological implications of the model are discussed, and methods for relating the model to real cell systems by means of commonly used experimental techniques are described. The model is compared with earlier models.     

A model for cell type localization in the migrating slug of <Emphasis Type="Italic">Dictyostelium discoideum</Emphasis> based on differential chemotactic sensitivity to cAMP and differential sensitivity to suppression of chemotaxis by ammonia

The three basic cell types in the migrating slug of Dictyostelium discoideum show differential chemotactic response to cyclic AMP (cAMP) and differential sensitivity to suppression of the chemotaxis by ammonia. The values of these parameters indicate a progressive maturation of chemotactic properties during the transdifferentiation of slug cell types. We present a model that explains the localization of the three cell types within the slug based on these chemotactic differences and on the maturation of their chemotactic properties.     

Neighborhood aggregation effect and its effective scale on reproductive success in Shorea laxa (Dipterocarpaceae)

This study investigated whether reproductive success is affected by the intensity of neighborhood aggregation of adults in the tropical tree Shorea laxa. We focused on three processes in the early reproductive stages: seed maturation; seed survival (categorizing sound seed, predation by insects and predation by vertebrates) in pre-seed dispersal; and seedling survival in the post-seed dispersal stage. We used a model selection procedure to examine the aggregation effect on reproductive success. The intensity of neighborhood aggregation was represented by the neighborhood aggregation index, which contains the adult number within a specific radius and the distances to neighboring adults (weight of proximity). Then, we evaluated the models exhaustively with the aggregation index having different scales (radius and weight of proximity) to assess the scale on which aggregation had significant effects. In particular, the best effective neighborhood scale, which is defined as the scale of the index in the model with minimum Akaike information criterion, was examined to compare those scales among processes. We found that the probability of seed maturation, seed survival and seedling survival decreased with the aggregation index at specific scales. This suggests that aggregation influenced reproductive success negatively in both the pre- and post-seed dispersal stages. However, the selected radii differed among processes: >200 and 130 m in pre- and post-seed dispersal stages, respectively. The selected weight of proximity also seemed to have a weak effect on all processes and was not different among processes.     

Targeted deletion of sprA from the tobacco plastid genome indicates that the encoded small RNA is not essential for pre-16S rRNA maturation in plastids

The small plastid RNA (spRNA) which includes a segment that is complementary to the pre-16S rRNA has been suggested to facilitate maturation of pre-16S rRNA in tobacco. To investigate the function of spRNA, the gene encoding it (sprA) was removed from the plastid genome using targeted gene deletion. We report here that deletion of sprA does not significantly affect pre-16S rRNA maturation, nor does it cause any obvious phenotype. Although the spRNA still may be involved in rRNA maturation, it is non-essential under normal growth conditions. Received: 29 May 1997 / Accepted: 6 August 1997     

Mathematical analysis of the oncornavirus maturation process (virion RNA conversion and morphological condensation)

The rate of the maturation process of avian myeloblastosis virus experimentally estimated on the basis of genomic viral RNA conversion and morphological transition of virions was mathematically analysed. Three mathematical models were suggested and fitted to experimental data. It was found that: (a) model of simple kinetics (Model 1) does not agree with experimental data. Therefore, two hypotheses were considered in further mathematical modelling: (b) virions are identical in time of budding: maturation is dependent on the presence of a virion component which is degraded with time (Model 2). This model agrees with experimental data in all stages of the maturation process. (c) Virions are released from cells at different stages of assembly (Model 3). This model differs from experimental data especially in early stages of maturation. The hypothesis used for the construction of Model 2 seems to be the most plausible to explain the maturation process and is in agreement with data of murine leukemia virus maturation which was found to be accomplished by cleavage of p70 precursor protein.     

Kinetics of antigen-induced phenotypic and functional maturation of human monocyte-derived dendritic cells.

Dendritic cells (DCs), a critical component of innate immunity, are the most potent APCs. When DCs mature, they can elicit strong T cell responses. We studied the kinetics of Ag-induced phenotypic and functional maturation of human monocyte-derived DCs using an in vitro T cell-independent culture system. With this model, we herein show that an Ag that has recently or repetitively been exposed ("exposed Ag") rapidly induces a high level of maturation; however, an Ag that has never or only remotely been exposed ("unexposed Ag") slowly induces a low level of maturation. The kinetics of Ag-induced maturation of DCs possibly implies a novel mechanism for immunological memory that would provide maximal host protection from repetitively invading pathogens in the environment.     

Food-dependent growth leads to overcompensation in stage-specific biomass when mortality increases: the influence of maturation versus reproduction regulation

We analyze a stage-structured biomass model for size-structured consumer-resource interactions. Maturation of juvenile consumers is modeled with a food-dependent function that consistently translates individual-level assumptions about growth in body size to the population level. Furthermore, the model accounts for stage-specific differences in resource use and mortality between juvenile and adult consumers. Without such differences, the model reduces to the Yodzis and Innes (1992) bioenergetics model, for which we show that model equilibria are characterized by a symmetry property that reproduction and maturation are equally limited by food density. As a consequence, biomass production rate exactly equals loss rate through maintenance and mortality in each consumer stage. Stage-specific differences break up this symmetry and turn specific stages into net producers and others into net losers of biomass. As a consequence, the population in equilibrium can be regulated in two distinct ways: either through total population reproduction or through total population maturation as limiting process. In the case of reproduction regulation, increases in mortality may lead to an increase of juvenile biomass. In the case of maturation regulation, increases in mortality may increase adult biomass. This overcompensation in biomass occurs with increases in both stage-independent and stage-specific mortality, even when the latter targets the stage exhibiting overcompensation.