Experimental assessment of the probabilistic maturation reaction norm: condition matters

The probabilistic maturation reaction norm (PMRN) describes an individual''s probability of maturing at a given age as a function of size and other relevant phenotypic traits. Population-level shifts in the PMRN are often interpreted to indicate genetic as opposed to phenotypic changes in maturation in fish. Inferences derived from trends in the PMRN have been challenged, warranting an experimental assessment of the method. This was accomplished in a laboratory experiment using zebrafish (Danio rerio). Fish were reared under different food levels to induce variation in growth and maturation. Plasticity in maturation was not entirely captured by the demographic age- and length-based PMRN. Adding condition to the PMRN captured a greater amount of environmental variation in maturation probability. Nevertheless, significant differences in the PMRNs among the food levels remained after accounting for the influences of age, size and condition on maturation probability indicating plasticity of the PMRN. This was particularly pronounced between fish held on low food levels as compared with fish experiencing abundant resources, with the latter experiencing higher size-specific maturation probabilities. Our analysis emphasizes the need for incorporating salient physiological traits influencing maturation, such as condition, to make accurate inferences about documented shifts observed in the position of PMRNs on maturation trends in wild fish stocks.     

Plasticity in probabilistic reaction norms for maturation in a salmonid fish

The relationship between body size and the probability of maturing, often referred to as the probabilistic maturation reaction norm (PMRN), has been increasingly used to infer genetic variation in maturation schedule. Despite this trend, few studies have directly evaluated plasticity in the PMRN. A transplant experiment using white-spotted charr demonstrated that the PMRN for precocious males exhibited plasticity. A smaller threshold size at maturity occurred in charr inhabiting narrow streams where more refuges are probably available for small charr, which in turn might enhance the reproductive success of sneaker precocious males. Our findings suggested that plastic effects should clearly be included in investigations of variation in PMRNs.     

HOW TO MEASURE MATURATION: A COMPARISON OF PROBABILISTIC METHODS USED TO TEST FOR GENOTYPIC VARIATION AND PLASTICITY IN THE DECISION TO MATURE

Maturation is a developmental trait that plays a key role in shaping organisms’ life‐history. However, progress in understanding how maturation phenotypes evolve has been held back by confusion over how best to model maturation decisions and a lack of studies comparing genotypic variation in maturation. Here, we fitted probabilistic maturation reaction norms (PMRNs) to data collected from five clones of Daphnia magna and five of Daphnia pulex collected from within and between different populations. We directly compared the utility of modeling approaches that assume maturation to be a process with an instantaneous rate with those that do not by fitting maturation rate and logistic regression models, and emphasize similarities and differences between them. Our results demonstrate that in Daphnia, PMRNs using a logistic regression approach were simpler to use and provided a better fit to the data. The decision to mature was plastic across a range of growth trajectories and dependent upon both body size and age. However, the age effect was stronger in D. magna than D. pulex and varied considerably between clones. Our results support the idea that maturation thresholds can evolve but also suggest that the notion of a threshold based on a single fixed state is an oversimplification that underestimates the adaptability of these important traits.     

Fish length exclusively determines sexual maturation in the European whitefish Coregonus lavaretus species complex

The probability that a fish matures at a certain age and length (the so‐called probabilistic maturation reaction norm, PMRN) was analysed for a European whitefish Coregonus lavaretus species complex population living in the Austrian pre‐alpine Lake Irrsee. Fish length was found to be the only relevant determinant of maturation probability, and females matured at slightly smaller sizes than males.     

Correlated contemporary evolution of life history traits in New Zealand Chinook salmon, Oncorhynchus tshawytscha

Size at age and age at maturity are important life history traits, affecting individual fitness and population demography. In salmon and other organisms, size and growth rate are commonly considered cues for maturation and thus age at maturity may or may not evolve independently of these features. Recent concerns surrounding the potential phenotypic and demographic responses of populations facing anthropogenic disturbances, such as climate change and harvest, place a premium on understanding the evolutionary genetic basis for evolution in size at age and age at maturity. In this study, we present the findings from a set of common-garden rearing experiments that empirically assess the heritable basis of phenotypic divergence in size at age and age at maturity in Chinook salmon (Oncorhynchus tshawytscha) populations introduced to New Zealand. We found consistent evidence of heritable differences among populations in both size at age and age at maturity, often corresponding to patterns observed in the wild. Populations diverged in size and growth profiles, even when accounting for eventual age at maturation. By contrast, most, but not all, cases of divergence in age at maturity were driven by the differences in size or growth rate rather than differences in the threshold relationship linking growth rate and probability of maturation. These findings help us understand how life histories may evolve through trait interactions in populations exposed to natural and anthropogenic disturbances, and how we might best detect such evolution.     

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.     

Green swordtails alter their age at maturation in response to the population level of male ornamentation

Effects of the social environment on age at sexual maturation are assumed to require direct interactions, such as suppression of subordinates through aggression from dominants. Using green swordtails (Xiphophorus helleri), we demonstrate for the first time that females and males adjust their age at maturation in response to visual cues of male sexual ornamentation in the current environment: females matured earlier, whereas males matured later if all the mature males seen had large ornaments. Thus, age at maturation shifted in accordance with the perceived quality of mates (females) or mating competitors (males), demonstrating a capability to use visual cues from the environment to strategically adjust rates of sexual development.     

Endocrine and developmental correlates of unilateral cryptorchidism in a wild baboon

A wild, group-living 8.5-year-old adult baboon was found to have only a single palpable testicle, the only case of cryptorchidism found among more than 200 males that we have examined. This young adult had an unusually small body size for his age, one that was comparable to that of immature males two years younger, and during maturation his body mass was increasingly small for his age. As a young adult, he also had very low testosterone concentrations, which, in combination with his small size, history of impaired growth, and the absence of any obvious scars around the scrotum, suggest that this is a case of spontaneous unilateral cryptorchidism of unknown cause rather than one of monorchidism arising from injury. Despite striking differences in his growth, adult body size, and testosterone levels, the male's cryptorchidism seemed to have relatively little effect on his social and sexual maturation in his natal group. Nonetheless, it may be related to his inability to gain entry into another group after dispersal.     

Fish age at maturation is influenced by temperature independently of growth

Age and size at maturation are important correlates of fitness in many organisms and understanding how these are influenced by environmental conditions is therefore required to predict populations’ responses to environmental changes. In ectotherms, growth and maturation are closely linked to temperature, but nonetheless it is often unclear how temperature-induced variation in growth and temperature per se translate to the process of maturation. Here, we test this explicitly with a common garden experiment using nine-spined sticklebacks (Pungitius pungitius). We reared fish in 14 and 17°C and recorded high resolution growth trajectories and the timing of maturation on an individual basis. To characterize the growth of each individual, we fitted a von Bertalanffy growth curve to each measured growth trajectory, so that the three parameters of the curve provided a summary of an individual’s growth. Temperature treatments induced changes in both the growth parameters and the age at maturation. In females, changes in the age of maturation were encompassed by variations in growth, whereas in males there was a temperature-related shift in the age at maturation that was unrelated to growth. Our experiment demonstrates that temperature can affect maturation directly, and not only through temperature-induced changes in growth. Therefore, one cannot predict, on the basis of growth only, how changes in temperature might alter age and size at maturation and the subsequent reproduction.     

Genetic and social control of male maturation in Phallichthys quadripunctatus (Pisces: Poeciliidae)

Age and size at maturity can have significant fitness consequences. Selection often favors early-maturing individuals because of their higher survival to maturity and greater relative contribution to population growth rate, but it may also favor delayed maturation if fitness increases with age or size at maturity. Males of several poeciliid fishes exhibit variation in age and size at maturity primarily controlled by a sex-linked gene called the P-locus. Wild-caught Phallichthys quadripunctatus males show a bimodal size distribution, which is often associated with a P-locus polymorphism in other poeciliids. We conducted two experiments to evaluate the inheritance of male age and size at maturity and the influence of social environment (presence of mature or juvenile males during development) on these traits. We specifically tested the hypothesis that male age and size at maturity in P. quadripunctatus are governed by a single Y-linked locus, and modified by the social environment. Although our results imply both a genetic and an environmental component to the dimorphism in maturation, both large and small males were able to sire both large and small sons, allowing us to reject the hypothesis that age and size at maturity in this species are controlled by a single, Y-linked locus. Our data do not conform adequately to any of the genetic mechanisms described to date for maturation polymorphism in poeciliids. We suggest alternative mechanisms that may operate in P. quadripunctatus.     

The association between treatment parameters on the day of gonadotropin-releasing hormone antagonist initiation during a flexible protocol and oocyte maturation rate

This study aimed to evaluate the effects of different treatment parameters on the day of GnRH antagonist initiation on oocyte maturation rate. We performed a retrospective cohort study of women aged ≤ 38 who underwent their first IVF-ICSI treatment using a flexible GnRH antagonist protocol in a single university-affiliated medical center during 2005-2015. Treatment parameters of three groups of oocyte maturation rates (<60%, 60-90%,>90%) were compared. Multivariate analysis was conducted to detect an association between treatment parameters on the day of GnRH antagonist initiation and oocyte maturation rate. The cohort included 458 patients, of whom 180 (39%) had a high oocyte maturation rate (≥90%), 211 (46%) had an oocyte maturation rate between 60-90% and 67 (15%) had a low maturation rate (≤60%). Women with a high maturation rate had longer duration of treatment (10.3 ± 2.9 days vs. 9.6 ± 2.5 vs. 9.5 ± 3.2, P = 0.019), lower levels of estradiol (1985 ± 1357 vs. 2406 ± 1666 vs. 2325 ± 1811, P = 0.027) and lower estradiol/maximal follicular diameter ratio on the day of GnRH antagonist initiation (137 ± 89 vs. 165 ± 103 vs. 163 ± 125, P = 0.019) as compared to women with medium and low maturation rates, respectively. Using linear regression multivariate analysis, lower estradiol and lower estradiol/maximal follicular diameter ratio on GnRH antagonist initiation day were associated with higher oocyte maturation rate. Further prospective studies to determine the best timing for GnRH antagonist initiation are needed.     

Effects of follicle-stimulating hormone and ovarian steroids during vitro meiotic maturation on fertilization of rat oocytes

The present study examined the effects of gonadotropins and ovarian steroids during in vitro meiotic maturation of rat oocytes on their ability to undergo in vitro fertilization. Fully grown oocytes were isolated from antral follicles of immature rats and cultured as oocyte-cumulus cell complexes (OCC) under conditions in which completion of meiotic maturation occurs spontaneously. They were then exposed to spermatozoa under conditions in which oocytes matured in vivo exhibit high fertilization rates. Compared with oocytes from pregnant mare's serum gonadotropin (PMSG) or follicle-stimulating hormone (FSH)-treated rats, a simiiar proportion of the oocytes (>80%) from untreated rats underwent germinal vesicle breakdown, but such oocytes had a lower rate of fertilization (70% vs. 20%). The presence of FSH during in vitro maturation restored the fertilization rate for oocytes from untreated rats, while a cytochrome P450 inhibitor, aminoglutethimide phosphate abolished this beneficial effect of FSH. The addition of progesterone during the in vitro maturation period duplicated the beneficial effect of FSH on fertilization rate of oocytes from untreated rats; oestradiol-17β was less effective in this regard, and 5α-dihydrotestosterone was ineffective. These findings indicate that FSH and progesterone, although having no apparent effect on nuclear maturation of the oocyte, play an important role during oocyte maturation in enabling normal fertilization to occur.     

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 ontogeny of territoriality during maturation

Territoriality drives the evolution of many mating systems, yet has remained an extremely difficult trait to measure in the wild. Classic studies rely on the theoretical framework of resource holding potential (RHP) as a predictor of success in territory acquisition. However, mounting evidence suggests that an individual's RHP may change over short time scales. Previous studies suggest that RHP is best understood by considering two categories of territoriality, resource defending and resource usurping potential (RDP and RUP, respectively). In a population of the side-blotched lizard, Uta stansburiana, blue-throated males defend territories near their natal site (RDP) while mature orange-throated males use their RUP to sequester high quality territories from defending territorial males. We tested differences in territoriality by releasing pairs of maturing male lizards onto experimentally altered territories that had improved thermal qualities owing to the addition of rock piles. Dyads of males competed for these thermal resources and the females that were released on rock piles. Early in the season, when throat colors were not yet fully expressed, large male body size predicted contest victories irrespective of throat color. This pattern changed however, with the onset of the breeding season and maturation of throat color. Orange males tended to usurp territories from blue males within 2 weeks of contest initiation. Large male body size still influenced these contests, but after one more week, throat color was the sole factor explaining variance in territory ownership. We demonstrate the ontogeny of territoriality relating to body size and throat color during maturation, and suggest a novel approach to assessing territoriality and aggression in the wild.     

Induction of meiotic maturation in mouse oocytes by adenosine analogs

In this study we have examined the meiosis-inducing influence of adenosine analogs in mouse oocytes. When a varied group of nucleosides and nucleotides were tested on overnight cultures of hypoxanthine-arrested, cumulus cell-enclosed oocytes (CEO), halogenated adenosine nucleosides, but not native adenosine, exhibited a significant meiosis-inducing capability. When tested under a variety of conditions, meiotic induction by 8-bromo-adenosine (8-Br-Ado) and a second adenosine analog, methylmercaptopurine riboside (MMPR), was especially potent in denuded oocytes (DO) compared to CEO and was not dependent on the type of inhibitor chosen to maintain meiotic arrest. Germinal vesicle breakdown (GVB) was stimulated with rapid kinetics and was preceded by an increase in AMP-activated protein kinase (AMPK) activity. Moreover, compound C, an inhibitor of AMPK, blocked the meiosis-inducing activities of both adenosine analogs. When tested for an effect on meiotic progression to metaphase II (MII) in spontaneously maturing CEO, 8-Br-Ado and the AMPK activator, 5-aminoimidazole-4-carboxamide 1-beta-D-ribofuranoside (AICAR), increased the percentage of MII-stage oocytes, but MMPR decreased this number. Adenosine and inhibitors of de novo purine synthesis had no effect on the completion of maturation, while compound C suppressed this process. These results support the proposition that oocyte AMPK mediates the positive influence of AICAR and 8-Br-Ado on both the initiation and completion of meiotic maturation. The role of AMPK in MMPR action is less clear.     

Influence of Male Presence on Sexual Maturation in Female Caribbean Fruit Fly, Anastrepha suspensa (Diptera: Tephritidae)

The presence of males was shown to affect the rate of female ovarian development in the Caribbean fruit fly, Anastrepha suspensa (Loew). Virgin females were maintained either in the absence or presence of males. Those sharing a common space with males had either visual contact with the opposite sex or no visual contact. Three strains of Caribbean fruit fly were tested: mass reared strain (flies in colony for more than 20 years); semi-wild strain, flies recently adapted to the laboratory conditions (ca. 12 months); and a wild strain collected in the field. We found that: (1) Mass reared, semi-wild, and wild strains had different female maturation rates, as measured by the presence of mature oocytes, regardless of male presence. (2) Male presence accelerated maturation in wild females and to a lesser extent in semi-wild flies, but had no effect on the long-domesticated mass reared strain. (3) A barrier between female and male cages removed any possibility of visual communication but had no effect on the males’ effect on female maturation. We discuss the adaptive significance of facultative ovarian maturation and the use of male-produced cues to regulate sexual development, and comment on the rapid rate of selection on female maturation under mass-rearing conditions.     

The growth pattern of chimpanzees: Somatic growth and reproductive maturation inPan troglodytes

Growth of chimpanzees reared at the Kumamoto Primates Park of Sanwa Kagaku Kenkyusho Co. Ltd. was studied cross-sectionally from the viewpoints of somatic growth and reproductive maturation. Distance and velocity curves were expressed using spline function method. Males showed adolescent growth acceleration in body weight, with a peak at 7.86 yrs of age, but not in trunk length. Females showed continuous rapid growth from mid-juvenile to adolescent phase in both body weight and trunk length, but no isolated adolescent spurt. The Sanwa chimpanzees matured at about 12.5 yrs of age for females and 15.0 yrs for males. The mean adult weights and trunk lengths were 53.2 kg and 507.8 mm for males and 42.7 kg and 481.6 mm for females. The Sanwa chimpanzees had similar growth patterns to those of the Yerkes chimpanzees, although they showed a slight delay in infancy, and a higher growth rate from the early juvenile phase onwards. Growth patterns in these two laboratories may be regarded as “normative” for laboratory-reared chimpanzees. They matured earlier than wild chimpanzees by more than two years. The major reason for the retarded maturation in wild chimpanzees is the delay of growth from infant to the early juvenile phases (0–4 yrs of age), probably owing to a limited nutritional supply from the mother. Development of the testes comprised three phases: slow growth from infant to juvenile (until 6.4 yrs); rapid growth around adolescence (until 9.2 yrs); and adult (mean testicular volume, 187 cm³). Setting the nutritional standard at 2,000–2,600 Cal/day (= Kcal/day) per adult, calories were considered for captive chimpanzees in each age class.     

Probabilistic maturation reaction norms assessed from mark–recaptures of wild fish in their natural habitat

Reaction norms are a valuable tool in evolutionary biology. Lately, the probabilistic maturation reaction norm approach, describing probabilities of maturing at combinations of age and body size, has been much applied for testing whether phenotypic changes in exploited populations of fish are mainly plastic or involving an evolutionary component. However, due to typical field data limitations, with imperfect knowledge about individual life histories, this demographic method still needs to be assessed. Using 13 years of direct mark–recapture observations on individual growth and maturation in an intensively sampled population of brown trout (Salmo trutta), we show that the probabilistic maturation reaction norm approach may perform well even if the assumption of equal survival of juvenile and maturing fish does not hold. Earlier studies have pointed out that growth effects may confound the interpretation of shifts in maturation reaction norms, because this method in its basic form deals with body size rather than growth. In our case, however, we found that juvenile body size, rather than annual growth, was more strongly associated with maturation. Viewed against earlier studies, our results also underscore the challenges of generalizing life‐history patterns among species and populations.     

Physical maturation and age estimates of yellow baboons,Papio cynocephalus,in Amboseli National Park,Kenya

In a longitudinal study of individually identified wild baboons in Amboseli National Park, Kenya, we collected data on physical development and reproductive maturation. Confirming and extending our earlier results, we demonstrated that the ratio of ages at which developmental milestones occur in the field as compared to those under extensive provisioning or in captivity were approximately 5:3. The age range for some developmental milestones was quite narrow and discrete, while for others there was considerable between-individual variability and more gradual changes. For infants, only the change from pink to gray of the paracallosal skin occurred within a brief age span. For older animals two important developmental events are readily identified and occur within a fairly narrow age range: Rapid enlargement of testes at 5 to 6 years for males and onset of menarche at 4 to 5 ½ years for females. In the present report, we considered some consequences of accelerated or delayed maturation. We further explored the need to employ different age-class criteria for different research problems.     

Evidence for genetic differentiation in timing of maturation among nine‐spined stickleback populations

Timing of maturation is an important life‐history trait that is likely to be subjected to strong natural selection. Although population differences in timing of maturation have been frequently reported in studies of wild animal populations, little is known about the genetic basis of this differentiation. Here, we investigated population and sex differences in timing of maturation within and between two nine‐spined stickleback (Pungitius pungitius) populations in a laboratory breeding experiment. We found that fish from the high‐predation marine population matured earlier than fish from the low‐predation pond population and males matured earlier than females. Timing of maturation in both reciprocal hybrid crosses between the two populations was similar to that in the marine population, suggesting that early timing of maturation is a dominant trait, whereas delayed timing of maturation in the pond is a recessive trait. Thus, the observed population divergence is suggestive of strong natural selection against early maturation in the piscine‐predator‐free pond population.