Zebra finch males compensate in plumage ornaments at sexual maturation for a bad start in life

Background

An individual's fitness in part depends on the characteristics of the mate so that sexually attractive ornaments, as signals of quality, are used in mate choice. Often such ornaments develop already early in life and thus are affected by nutritional conditions experienced then. Individuals thus should benefit by compensating as soon as possible for poor initial development of ornaments, to be attractive already at sexual maturity. Here, we tested whether early nutritional stress affects the cheek patch size of male Zebra finches (Taeniopygia guttata), which are important in mate choice, and whether a small cheek patch size early on is compensated at sexual maturation. Furthermore we tested whether exploration behaviour is affected by such a compensation, as shown for other compensatory growth trajectories.

Results

Zebra finch males which were raised under poorer nutritional conditions initially expressed smaller cheek patches at day 50 post-hatching but then compensated in cheek patch size already at 65 days, i.e. when becoming sexually mature. Furthermore, compensatory growth in cheek patch during adolescence was negatively correlated with activity and exploration behaviour, measured in a novel environment.

Conclusion

This compensation in cheek patch size benefits male attractiveness but also was related to less exploration behaviour, an established proxy for avian personality traits. We discuss the possibility that compensatory priorities exist so that not all deficits from a bad start are caught-up at the same time. Resource allocation to compensate for poorly expressed traits is likely to have evolved to optimise traits by the time they are most beneficial.

     

Seasonal variations in male mice at the time of sexual maturation

The sexual maturation of male mice reared under constant laboratory conditions was studied in animals born in different months of the year. The body weights were significantly affected by the month of birth. Males born in March and May were heavier at 4 and 5 weeks of age than those born in autumn and winter. As indicated by the relative weights of accessory glands, males born in spring matured earlier compared with animals born in other months of the year. Variation in the relative testicular weights during maturation was not influenced by the month of birth. Female mice also showed a significant relationship between the month of birth and sexual maturation. Females born in March reached puberty, as measured by the age of vaginal opening and first oestrus, earlier than those born in other months of the year.     

Exercise-induced hormone responses in girls at different stages of sexual maturation

The dependence of exercise-induced hormone responses on sexual maturation was tested in a 3-year longitudinal experiment on 34 girls (aged 11–12 years at the beginning). Sexual maturation was evaluated by Tanners five-stage scale. Children cycled for 20-min at 60% maximal oxygen uptake once a year. Cortisol, insulin, growth hormone, β-oestradiol, progesterone and testosterone concentrations in venous blood were determined by radioimmunoassay procedures. Basal concentrations of growth hormone increased and of cortisol decreased when breast stage III was reached. Reaching breast stage IV was associated with an increase in basal concentrations of β-oestradiol, progesterone and testosterone. The exercise induced significant increases in concentrations of cortisol, growth hormone and β-oestradiol and a decrease in insulin concentration. At breast stage III the increase in cortisol concentration was to a lower level [467 (SEM 42) vs 567 (SEM 46)nmol · l⁻¹] and growth hormone concentration to a higher level [29.4 (SEM 0.5) vs 12.8 (SEM 0.4)ng · ml⁻¹], while the fall in insulin concentration was less pronounced [postexercise level 10.6 (SEM 0.9) vs 7.8 (SEM 0.8)mU · l⁻¹] than in stage II. The magnitude of the cortisol response was reduced in the last stage of breast development (+42.1% vs +55.5% at stage II, +66.2% at stage III, and +50.0% at stage IV). The magnitude of β-oestradiol response was the lowest in breast stage IV (+15.8%) and the highest at stage V (+41.1%). The progesterone response became significant at stage IV and testosterone response at stage V. In conclusion, we found that reaching breast stage III was associated with altered responses of cortisol, insulin and growth hormone concentrations while the responses of the sex hormone concentrations became pronounced in the last stages of sexual maturation. Accepted: 17 September 1997     

Relationships between handling,behaviour and stress in lambs at abattoirs

There is community concern about the treatment of farm animals post-farm gate, particularly animal transport and slaughter. Relationships between lamb behavioural and physiological variables on farm, stockperson, dog and lamb behavioural variables pre-slaughter and plasma cortisol, glucose and lactate in lambs post-slaughter were studied in 400 lambs. The lambs were observed in three behavioural tests, novel arena, flight distance to a human and temperament tests, before transport for slaughter. Closed-circuit television video footage was used to record stockperson, dog and lamb behaviour immediately before slaughter. Blood samples for cortisol, glucose and lactate analyses were collected on farm following the three behavioural tests and immediately post-slaughter. The regression models that best predicted plasma cortisol, glucose and lactate concentrations post-slaughter included a mixture of stockperson and dog behavioural variables as well as lamb variables both on-farm and pre-slaughter. These regression models accounted for 33%, 34% and 44% of the variance in plasma cortisol, glucose and lactate concentrations post-slaughter, respectively. Some of the stockperson and dog behaviours pre-slaughter that were predictive of the stress and metabolic variables post-slaughter included the duration of negative stockperson behaviours such as fast locomotion and lifting/pulling lambs, and the duration of dog behaviours such as lunging and barking at the lamb, while some of the predictive lamb behaviour variables included the durations of jumping and fleeing. Some of the physiological and behavioural responses to the behavioural tests on farm were also predictive of the stress and metabolic variables post-slaughter. These relationships support the well-demonstrated effect of handling on fear and stress responses in livestock, and although not direct evidence of causal relationships, highlight the potential benefits of training stockpeople to reduce fear and stress in sheep at abattoirs.     

The influence of the parental environment on sexual maturation in male mice

Experiments were designed to examine the influence of either one or both parents on the sexual maturation of male mice. A pregnant female and an adult vasectomized male were housed together and, at delivery, the litter was reduced to 6 pups, 3 of each sex. After weaning, mother, foster-father or both, stayed in cohabitation with their pups until sacrifice. The results showed that: (1) the permanent presence of one or both parents did not affect either testicular growth or the age at first fertile matings. (2) in maturing males (30-40 days), seminal vesicle growth was accelerated by the presence of the mother, inhibited by the presence of the foster-father. (3) in maturing males, the presence of one or both parents lowered plasma testosterone levels. On the opposite, in 90-day-old males, the same conditions increased testosterone levels. These results indicate that only the endocrine function of the testis is affected by the parental environment. The effects are age-dependent.     

Regulatory roles of leptin at the hypothalamic-hypophyseal axis before and after sexual maturation in cattle

Studies assessed, either directly or indirectly, the role of GnRH in leptin-mediated stimulation of LH release in cattle before and after sexual maturation. In experiment 1, the objectives were to determine whether leptin could acutely accelerate the frequency of LH pulses, and putatively GnRH pulses, in prepubertal heifers at different stages of development. In experiment 2, we determined directly whether acute, leptin-mediated increases in LH secretion in the fasted, mature female are accompanied by an increase in GnRH secretion. Ten-month-old prepubertal heifers (experiment 1) fed normal- (n = 5) and restricted-growth (n = 5) diets received three injections of saline or recombinant ovine leptin (oleptin; 0.2 microg/kg body weight, i.v.) at hourly intervals during 5-h experiments conducted every 5 wk until all normal-growth heifers were pubertal. Leptin increased mean concentrations of circulating LH regardless of diet, but pulse characteristics were not altered at any age. In experiment 2, ovariectomized, estradiol-implanted cows (n = 5) were fasted twice for 72 h and treated with either saline or oleptin i.v. (as in experiment 1) on Day 3 of each fast. Leptin increased plasma concentrations of LH and third ventricle cerebrospinal fluid concentrations of GnRH, and increased the amplitude of LH and the size of GnRH pulses, respectively, on Day 3 of fasting compared to saline. Overall, results indicate that leptin is unable to accelerate the pulse generator in heifers at any developmental stage. However, leptin-mediated augmentation of LH concentrations and pulse amplitude in the nutritionally stressed, mature female are associated with modifications in GnRH secretory dynamics.     

Nutritional influences on sexual maturation in the rat

The effect of altered nutrition on sexual maturation may depend in part on the nature and timing of the dietary change. The data are conflicting as to whether rats undernourished before weaning but normally fed after weaning have delayed puberty, but such undernourished rats clearly weigh less at vaginal opening than do normally fed animals. Altered nutrition after weaning can change the timing of puberty, and in such cases the body weight at puberty of the animals given the modified diet is frequently abnormal. The factors regulating the age and weight at puberty of rats fed altered diets seem to include the degree of underfeeding, as reflected in the growth rate, and the composition of the diet. Undernourished immature male rats have low serum testosterone secondary to gonadotropin deficiency. Basal luteinizing hormone (LH) in these animals is either low or "inappropriately normal" relative to their hypoandrogenic state (low serum testosterone and sexual accessory gland weights), and serum LH increases after luteinizing hormone-releasing hormone (LHRH) or castration are normal or minimally reduced. Serum follicle-stimulating hormone (FSH) in undernourished rats is subnormal basally and after administration of LHRH, but not after castration, which suggests that the low basal serum FSH is due to inhibition of FSH output by a testicular factor. Spermatogenesis may be unaltered by dietary changes severe enough to cause hypoandrogenism, although very severe under-nutrition will impair sperm production.     

The period of sexual maturation and the age at mating in Iridomyrmex humilis, an ant with intranidal mating

The process of sexual maturation was studied in the ant Iridomyrmex humilis. Spermatogenesis starts during the pupal stage and sperm is transferred to the seminal vesicles during the first four days after emergence. The testes start to degenerate early in the pupal stage and totally shrivel up during the first days after emergence. Males therefore have a fixed amount of sperm. Both males and females reach sexual maturity only 2–3 days after emergence; some of them mate as early as the first day after emergence. Overall, it appears that the length of time needed to reach sexual maturity in ants is highly correlated with the mode of colony founding. The maturation period is much longer in those species in which young queens initiate colonies without the help of workers (independent founding) than in those where young queens need the help of workers (dependent founding). This is probably associated with the fact that independent founding queens require large amounts of energy reserves in order to found colonies; these energy reserves are accumulated after emergence. In contrast, dependent founding queens do not accumulate as many energy reserves and are therefore sexually receptive at a younger age.     

Sea growth, smolt age and age at sexual maturation in Atlantic salmon

Relationships between growth at sea, smolt size and age at sexual maturation of Atlantic salmon Salmo salar were tested. The fish were offspring of brood stocks sampled in eight Norwegian rivers at latitudes between 59° and 70° N, hatchery reared and released at smolting at the mouth of the River Imsa (59° N). Smolt size influenced the subsequent growth rate of Atlantic salmon. The larger the fish were at release, the slower the yearly length increment at sea. Mean sea age at sexual maturity, measured as proportion of the returning adults attaining sexual maturity at sea age 2 years, was significantly correlated with mean growth rate during the first year at sea and mean smolt size ( r ²= 0·74, P < 0·001). Fish attaining maturity at a relatively high sea age were more fast growing during their first year at sea than those maturing at a younger age. The results indicate that high sea age at sexual maturation is a population-specific characteristic and associated with high early growth rate at sea.     

Postnatal maturation of respiration in intact and carotid body-chemodenervated lambs

The contribution of the carotid body chemoreceptor to postnatal maturation of breathing was evaluated in lambs from 7 to 70 days of age. The study was conducted by comparing the eupneic ventilation and resting pneumograms in intact conscious lambs with those of lambs that were carotid body chemodenervated (CBD) at birth. In comparison to the 1-wk-old intact lambs, the CBD lambs had significant decreases in minute ventilation (VE, 313 vs. 517 ml/kg), tidal volume (VT, 7.2 vs. 10.5 ml/kg), respiratory rate (f, 44 vs. 51 breaths/min), and occlusion pressure (P0.1, 2.8 vs. 7.2 cmH2O). Arterial PO2's were 59 vs. 75 Torr (P less than 0.05) and arterial PCO2's 47 vs. 36 Torr (P less than 0.05), respectively, in CBD and intact lambs. In intact lambs from 7 to 70 days, resting VE decreased progressively from 517 to 274 ml/kg (P less than 0.01) due to a fall in VT, mean inspiratory flow (VT/TI), and f, whereas the ratio of inspiratory time to total breath duration remained constant. P0.1 decreased from 7.2 to 3.9 cmH2O from 7 to 42 days. In contrast the CBD lambs experienced only minimal changes in VE, VT, VT/TI, and f during the same period. VE only decreased from 313 to 218 and P0.1 from 2.8 to 2.4 cmH2O. In contrast to that of intact lambs the resting pneumogram of CBD lambs remained relatively fixed from 7 to 70 days. Three CBD lambs died unexpectedly, without apparent cause, in the 4th and 5th wk of life.(ABSTRACT TRUNCATED AT 250 WORDS)     

Measuring probabilistic reaction norms for age and size at maturation

We present a new probabilistic concept of reaction norms for age and size at maturation that is applicable when observations are carried out at discrete time intervals. This approach can also be used to estimate reaction norms for age and size at metamorphosis or at other ontogenetic transitions. Such estimations are critical for understanding phenotypic plasticity and life-history changes in variable environments, assessing genetic changes in the presence of phenotypic plasticity, and calibrating size- and age-structured population models. We show that previous approaches to this problem, based on regressing size against age at maturation, give results that are systematically biased when compared to the probabilistic reaction norms. The bias can be substantial and is likely to lead to qualitatively incorrect conclusions; it is caused by failing to account for the probabilistic nature of the maturation process. We explain why, instead, robust estimations of maturation reaction norms should be based on logistic regression or on other statistical models that treat the probability of maturing as a dependent variable. We demonstrate the utility of our approach with two examples. First, the analysis of data generated for a known reaction norm highlights some crucial limitations of previous approaches. Second, application to the northeast arctic cod (Gadus morhua) illustrates how our approach can be used to shed new light on existing real-world data.     

The effect of sexual maturation on the spatial distribution of Baltic salmon

This study examines the migratory habits of tagged mature and immature Atlantic salmon parr Salmo salar released from the Norrfors hatchery on the River Umeälven, Sweden from 1975 to 1977 and 1988 to 1990. Tags were recaptured in the Baltic Main Basin, the Gulf of Bothnia, and in the Umeälven. Ninety-three per cent of previously mature males were recovered in the Umeälven compared with 23% of the previously immature smolts during the calendar year of release. In the second year after release (grilse year), the proportion of early maturing males recovered in the Umeälven was significantly greater than the proportion of previously immature smolts recovered in the Umeälven. Likewise, the proportion of previously mature males recovered in the Main Basin was significantly less than the proportion of previously immature smolts recovered in the Main Basin in the second calendar year after release. Previously mature males rematured after fewer years at sea, on average, than the previously immature smolts. Following the second calendar year after release, the proportions of previously mature males and previously immature smolts were not significantly different throughout the Baltic Sea.     

The importance of social dimension and maturation stage for the probabilistic maturation reaction norm in Poecilia reticulata

Maturation is an important event in an organism's life history, with important implications on dynamics of both wild and captive populations. The probabilistic maturation reaction norm (PMRN) has emerged as an important method to describe variation in maturation in wild fish. Because most PMRNs are based on age and size only, it is important to understand limitations of these variables in explaining maturation. We experimentally assessed (i) the sensitivity of age‐ and size‐based PMRNs to unaccounted sources of plasticity, (ii) the role of social environment on maturation and (iii) the significance of estimating PMRNs early and late in the maturation process (initiation and completion of maturation, respectively). We reared male guppies (Poecilia reticulata) under laboratory conditions, subjected to two food levels and three different social cues. We found that growth and social environment affected the maturation in a way that could not be accounted for by their effect on age and size. PMRNs estimated for the initiation stage were less plastic (growth differences and social cues influenced the PMRN shape only little) than those for completion. The initiation of maturation is probably closer to the maturation ‘decision’ and allows determining factors influencing maturation decision most accurately.     

The analysis of reaction norms for age and size at maturity using maturation rate models

Reaction norms for age and size at maturity are being analyzed to answer important questions about the evolution of life histories. A new statistical method is developed in the framework of time-to-event data analysis, which circumvents shortcomings in currently available approaches. The method emphasizes the estimation of age- and size-dependent maturation rates. Individual probabilities of maturation during any given time interval follow by integrating maturation rate along the growth curve. The integration may be performed in different ways, over ages or sizes or both, corresponding to different assumptions on how individuals store the operational history of the maturation process. Data analysis amounts to fitting generalized nonlinear regression models to a maturation status variable. This technique has three main advantages over existing methods: (1) treating maturation as a stochastic process enables one to specify a rate of maturation; (2) age and size at which maturation occurs do not have to be observed exactly, and bias arising from approximations and interpolations is avoided; (3) ages at which sizes are measured and maturation status are observed can differ between individuals. An application to data on the springtail Folsomia candida is presented. Models with age-dependent integration of maturation rates were preferred. The analysis demonstrates a significant size dependence of the maturation rate but no age dependence.     

Intra-amniotic endotoxin: chorioamnionitis precedes lung maturation in preterm lambs

The inflammatory and lung maturational effects of intra-amniotic exposure to endotoxin were assessed in fetal lambs. Five hours to 25 days after intra-amniotic injection of endotoxin, preterm lambs were delivered at 119-125 days gestation. Intra-amniotic endotoxin caused an inflammatory cell infiltration in amnion/chorion at 5 h, which persisted for 25 days. At 5-15 h after endotoxin, amnion/chorion cytokine mRNAs increased [12- to 26-fold for interleukin (IL)-1beta, IL-6, and IL-8 mRNA and 3-fold for tumor necrosis factor-alpha mRNA]. At 1-2 days after endotoxin, lung cytokine mRNAs increased 6- to 49-fold. Endotoxin caused modest changes in peripheral white blood cell counts and no significant cytokine mRNA responses in fetal liver, placenta, or jejunum. Lung maturation, as characterized by increased lung volumes and alveolar saturated phosphatidylcholine, occurred at 7 days and persisted for 25 days after endotoxin. We conclude that exposure to a single dose of intra-amniotic endotoxin causes inflammation and increases in cytokine mRNA in amnion/chorion and the fetal lung before lung maturation, consistent with the hypothesis that proinflammatory cytokines signal lung maturation.     

Characterization of Sertoli cell RNA synthetic activities in vitro at selected times during sexual maturation

In this study, Sertoli cell RNA synthetic activity in vitro was characterized at selected times during sexual maturation. Sertoli cells, isolated from rat testes undergoing the first wave of spermatogenesis and placed in culture for 4 days, exhibited 2-fold increases in soluble ribonucleotide pools and in total RNA concentrations over the age span of 18-35 days. High performance liquid chromatographic analysis of the ribonucleotide pools in Sertoli cells cultured from 18- and 33- to 34-day-old rats revealed that, in addition to the overall age-related doubling of concentrations, uridine triphosphate (UTP) and cytidine triphosphate (CTP) pools were disproportionately increased 4- and 6-fold, respectively. In general, Sertoli cell contained relatively small amounts of UTP in comparison to several other cell types, but exhibited a high ADP:ATP ratio. A uniform 2-fold increase in the base composition of Sertoli cell RNA per mg DNA was observed over the age span of 18-35 days, with no preferential increase in any one specific nucleotide. There was no change in [3H]uridine incorporation (2 h) into RNA per cell (pmol/mg DNA), but decreased specific activity of the RNA (pmol/mg RNA) in Sertoli cells cultured from 35-day-old rats as compared to those from 18- to 19-day-old rats. Similar differences were noted in the specific activity of label incorporated into specific RNA bases. In contrast, the specific activity of the UTP-CTP soluble pool/mg DNA was only slightly increased. These data indicate that processes related to RNA synthesis in the Sertoli cell undergo a number of changes during the period of sexual maturation.