Variation In Development Time Research Articles

Effects of temporal variation in temperature and density dependence on insect population dynamics

AbstractUnderstanding the effects of environmental variation on insect populations is important in light of predictions about increasing climatic variability. This paper uses the univoltine western corn rootworm (WCR, Diabrotica virgifera virgifera LeConte) as a case study and employs deterministic and stochastic modeling to evaluate how insect population dynamics is shaped by density‐dependent survival and annual variation in temperature, which are key in regulating insect populations. Field data showed that larval survival varied significantly between years but was constant for a range of densities. Survival dropped only beyond a threshold density, a feature resembling generalized Ricker functions used in modeling density‐dependent survival due to scramble competition for resources. We used soil temperature data for 20 yr to model annual variation in developmental time and survival. The deterministic model, where the developmental time was same across years, showed that though survival was high and did not change for a range of densities (i.e., density‐independent survival), predicted densities were large enough that strong density dependence could occur in the field (i.e., predicted densities fall in the region where survival drops sharply) and that populations could exhibit stable equilibrium, cycles, etc. Interestingly, populations with lower density‐independent survival were less likely to produce stable equilibrium compared to populations with higher density‐independent survival. We found that population densities were at stable equilibrium when both mean developmental time and fertility were relatively low or when developmental time and fertility were relatively high. This in turn implies that, in warmer regions, where mean developmental time will be lower, stability is more likely for insect populations with low fertility; species in warmer regions will experience cyclical and unstable dynamics when fertility is high. While increase in the mean developmental time reduces overall survival, increasing variation in developmental time could increase mean survival, a consequence of the Jensen's inequality, since survival was a concave decreasing function of developmental time. Hence, both mean and variability in temperature affect the dynamics of insect populations. Finally, we found that stochastic variation in soil temperature produced large variation in predicted population densities that could potentially enhance or diminish the effect of density dependence.

From fruitlet to harvest: Modelling and predicting size and its distributions for tomato, apple and pepper fruit

Size is an important property of all fruit as it determines, together with crop load, fruit yield. The aim of this study is to model the increase in fruit size during cell expansion based on diameter or length and to predict fruit size and volume, including the variation in size and volume, at harvest. The size of individual fruit during growth of fruit (four apple, two tomato and six pepper cultivars) was measured from early fruit set until harvest at several seasons. Size data were evaluated as diameter and length using the von Bertalanffy growth model, adapted to include the variation in size between individuals and the effect of growing temperature. The adapted von Bertalanffy model describes the increase in diameter and length and their variation. For any fruit type, size increased along the same generic growth model. A single stochastic variable, the biological shift factor, was sufficient to describe the variation in development time, initial size and maximum size. For all batches the percentage variation explained for were well over 93% with growth rate constants similar per species and only a minor effect of growing temperature.Prediction of the maximum size distribution based on measurements half way the cell expansion period is explored and discussed. Size and its distribution can be predicted based on a single measuring point in time but with two or three points in time the prediction system becomes more robust.

Anchors and snorkels: heterochrony, development and form in functionally constrained fossil crassatellid bivalves

AbstractNew growth rate estimates for nine species from three genera of New Zealand Crassatellidae (Mollusca: Bivalvia), combined with existing morphometric ontogenetic descriptions, allow identification of heterochronic processes in the evolution of these genera. Both paedomorphosis (progenesis and neoteny) and peramorphosis (hypermorphosis and acceleration) have occurred within the clade. Overall, morphological variability and response to environmental pressure in this nonsiphonate group is restricted by the interplay of anatomical and life habit constraints. Stability in the substrate, predator avoidance, sluggish burrowing speed, and inability to escape by deep burial are suggested as key drivers of, or constraints on, morphological change. Two groups of shell characters are identified: heavy, armored “anchors” and elongate “snorkels,” which combine juvenile and adult traits in shells of different sizes and ages, produced by heterochronic variation in developmental timing. Anchors and snorkels both represent different “solutions” to the problems of life as a nonsiphonate, infaunal bivalve.

The varied path to adulthood: Plasticity in developmental timing in hylobatids.

Maturation includes physical, reproductive, and social aspects that develop asynchronously. Intra- and inter-individual variation in the relative timing of each aspect reflects context-dependent plasticity. Plasticity in developmental timing may be important for the family-living small apes (family Hylobatidae), where reproductive opportunities are monopolized by territorial breeding pairs. Data on development in hylobatids are so far limited due to their elusive arboreal niche and long lifespans. Herein, we provide the first quantitative analysis of behavioral development in 14 captive individuals of three species (Hylobates moloch, Nomascus leucogenys, and Symphalangus syndactylus), with some individuals being observed over 8 years. To establish a baseline for behavioral development, we compare the behavior of infants (0-2 years), juveniles (2-4 years), adolescents (4-6 years), and subadults (6-9 years) in their natal groups from data obtained over 250 focal observation hours. We then relate changes in behavior to measures of somatic and physiological development, and to wild populations, to identify the degree of intra- and inter-individual variation in developmental timing. We found greater concordance between behavioral and physiological markers of weaning than between different markers of later development, and the timing of later milestones varied more among individuals. Behavioral estimates from both captive and wild individuals in their natal groups indicate that puberty begins close to age 5, but physiological maturation can occur 0.5-3 years earlier in captive individuals than in wild individuals. Ages at onset of puberty, sexual, and social maturation vary in both captive and wild populations. The available evidence indicates that the social environment during development (e.g., presence of breeding female and appropriate mating partner), as well as nutrition, play a role in the timing of life history transitions in hylobatids. Am. J. Primatol. 78:610-625, 2016. © 2015 Wiley Periodicals, Inc.

Morphological Consequences of Developmental Plasticity in Rana temporaria are not Accommodated into Among-Population or Among-Species Variation

Environmental induced developmental plasticity occurs in many organisms and it has been suggested to facilitate biological diversification. Here we use ranid frogs to examine whether morphological changes derived from adaptive developmental acceleration in response to pool drying within a species are mirrored by differences among populations and across species. Accelerated development in larval anurans under pool drying conditions is adaptive and often results in allometric changes in limb length and head shape. We examine the association between developmental rate and morphology within population, among populations in divergent environments, and among species inside the Ranidae frog family, combining experimental approaches with phylogenetic comparative analyses. We found that frogs reared under decreasing water conditions that simulated fast pool drying had a faster development rate compared to tadpoles reared on constant water conditions. This faster developmental rate resulted in different juvenile morphologies between the two pool drying conditions. The association between developmental rate and morphology found as a result of plasticity was not mirrored by differences among populations that differed in development, neither was it mirrored among species that differed in development rate. We conclude that morphological differences among populations and species were not driven by variation in developmental time per se. Instead, selective factors, presumably operating on locomotion and prey choice, seem to have had a stronger evolutionary effect on frog morphology than evolutionary divergences in developmental rate in the ranid populations and species studied.

Life history of the Antarctic tardigrade, Acutuncus antarcticus, under a constant laboratory environment

Tardigrades are found in most terrestrial and freshwater Antarctic ecosystems and are one of the most diverse and important groups of invertebrates in Antarctica. We developed a new laboratory system for rearing the Antarctic tardigrade Acutuncus antarcticus (Richters 1904), one of the most widespread and common Antarctic tardigrade species. To provide a description of the life history of this tardigrade, survival and reproduction of 68 individuals were observed and recorded daily at a constant temperature of 15 °C. The life-history data obtained are consistent with previous studies of other tardigrades. The exceptionally high hatching success obtained is suggested to be an important life-history characteristic of this species contributing to it often being a common and dominant species in the Antarctic habitats in which it occurs. Furthermore, high hatching success combined with very low variation in development time, under the protocol used in the current study, indicates that A. antarcticus may be a good model species for studies in developmental biology. Integrating data from this and previous studies, the importance of temperature on reproduction and growth in A. antarcticus was inferred. With terrestrial and freshwater ecosystems in some parts of Antarctica experiencing sometimes drastic contemporary climatic and environmental changes, studies of the effect of temperature on generation time and reproductive success in Antarctic tardigrades are urgently required, as these animals are important elements of community structure and function in polar ecosystems.

Kudzu-deprived First-generationMegacopta cribraria(F.) (Heteroptera: Plataspidae) Are Capable of Developing on Alternative Legume Species1

The biology of Megacopta cribraria (F.) (Heteroptera: Plataspidae) is not well understood in its new North American distribution, especially its development on alternative host plant species. We investigated whether overwintered M. cribraria could directly feed and oviposit on other legume species (Fabales: Fabaceae) without feeding on kudzu, Pueraria montana (Loureiro) Merrill var. lobata (Willdenow) Maesen & S. Almeida, and subsequently complete a first-generation on these species in no-choice greenhouse assays. Overwintered M. cribraria successfully oviposited on mung bean, Vigna radiata (L.) R. Wilczek; black-eyed pea, Vigna unguiculata (L.) Walp; lima bean ( = butter bean), Phaseolus lunatus L.; soybean, Glycine max L. Merrill; and kudzu. There were no differences in oviposition or the hatch rates on different legume species, although hatch rate was highest for soybean followed by kudzu, lima bean, mung bean, and black-eyed pea, respectively. First-generation M. cribraria developed on all legume species except black-eyed pea in 55.6 ± 1.6 d with little variation in developmental time of the instars. However, there were significantly more first instars molting to second instars on kudzu (19.6 ± 3.3), soybean (14.7 ± 3.0), and mung bean (19.0 ± 1.0) than on lima bean (5.3 ± 2.4). Mean developmental days of the first, second, and fourth instars were consistent at about seven days, while the third and fifth instars took longer to develop. Mortality from egg to adult was greatest on black-eyed pea, followed by lima bean, kudzu, mung bean, and soybean. These results indicate that overwintered M. cribraria adults are able to bypass kudzu to directly develop on soybean, lima bean, and mung bean crops.

Genetic moderation of child maltreatment effects on depression and internalizing symptoms by serotonin transporter linked polymorphic region (5-HTTLPR), brain-derived neurotrophic factor (BDNF), norepinephrine transporter (NET), and corticotropin releasing hormone receptor 1 (CRHR1) genes in African American children.

Genetic moderation of the effects of child maltreatment on depression and internalizing symptoms was investigated in a sample of low-income maltreated and nonmaltreated African American children (N = 1,096). Lifetime child maltreatment experiences were independently coded from Child Protective Services records and maternal report. Child depression and internalizing problems were assessed in the context of a summer research camp by self-report on the Children's Depression Inventory and adult counselor report on the Teacher Report Form. DNA was obtained from buccal cell or saliva samples and genotyped for polymorphisms of the following genes: serotonin transporter linked polymorphic region (5-HTTLPR), brain-derived neurotrophic factor (BDNF), norepinephrine transporter, and corticotropin releasing hormone receptor 1. Analyses of covariance with age and gender as covariates were conducted, with maltreatment status and respective polymorphism as main effects and their Gene × Environment (G × E) interactions. Maltreatment consistently was associated with higher Children's Depression Inventory and Teacher Report Form symptoms. The results for child self-report symptoms indicated a G × E interaction for BDNF and maltreatment. In addition, BDNF and triallelic 5-HTTLPR interacted with child maltreatment in a G × G × E interaction. Analyses for counselor report of child anxiety/depression symptoms on the Teacher Report Form indicated moderation of child maltreatment effects by triallelic 5-HTTLPR. These effects were elaborated based on variation in developmental timing of maltreatment experiences. Norepinephrine transporter was found to further moderate the G × E interaction of 5-HTTLPR and maltreatment status, revealing a G × G × E interaction. This G × G × E was extended by consideration of variation in maltreatment subtype experiences. Finally, G × G × E effects were observed for the co-action of BDNF and the corticotropin releasing hormone receptor 1 haplotype. The findings illustrate the variable influence of specific genotypes in G × E interactions based on variation in maltreatment experiences and the importance of a multigenic approach for understanding influences on depression and internalizing symptoms among African American children.

Mountain Pine Beetle Voltinism and Life History Characteristics across Latitudinal and Elevational Gradients in the Western United States

Substantial genetic variation in development time is known to exist among mountain pine beetle (Dendroctonus ponderosae Hopkins) populations across the western United States. The effect of this variation on geographic patterns in voltinism (generation time) and thermal requirements to produce specific voltinism pathways have not been investigated. The influence of voltinism on fitness traits, body size, and sex ratio is also unclear. We monitored mountain pine beetle voltinism, adult body size, sex ratio, and air temperatures at sites across latitudinal and elevational gradients in the western United States. With the exception of two sites at the coolest and warmest locations, the number of days required to complete a generation was similar. Thermal units required to achieve a generation, however, were significantly less for individuals at the coolest sites. Evolved adaptations explain this pattern, including developmental rates and thresholds that serve to synchronize cohorts and minimize cold-sensitive life stages in winter. These same adaptations reduce the capacity of mountain pine beetle at the warmest sites to take full advantage of increased thermal units, limiting the capacity for bivoltinism within the current realized distribution. Temperature was not correlated with adult size and sex ratio, and size was greatest in host trees other than lodgepole pine (Pinus contorta Dougl.). Our results provide baseline information for evaluating population responses in a changing climate.

Thermodynamics constrains allometric scaling of optimal development time in insects.

Development time is a critical life-history trait that has profound effects on organism fitness and on population growth rates. For ectotherms, development time is strongly influenced by temperature and is predicted to scale with body mass to the quarter power based on 1) the ontogenetic growth model of the metabolic theory of ecology which describes a bioenergetic balance between tissue maintenance and growth given the scaling relationship between metabolism and body size, and 2) numerous studies, primarily of vertebrate endotherms, that largely support this prediction. However, few studies have investigated the allometry of development time among invertebrates, including insects. Abundant data on development of diverse insects provides an ideal opportunity to better understand the scaling of development time in this ecologically and economically important group. Insects develop more quickly at warmer temperatures until reaching a minimum development time at some optimal temperature, after which development slows. We evaluated the allometry of insect development time by compiling estimates of minimum development time and optimal developmental temperature for 361 insect species from 16 orders with body mass varying over nearly 6 orders of magnitude. Allometric scaling exponents varied with the statistical approach: standardized major axis regression supported the predicted quarter-power scaling relationship, but ordinary and phylogenetic generalized least squares did not. Regardless of the statistical approach, body size alone explained less than 28% of the variation in development time. Models that also included optimal temperature explained over 50% of the variation in development time. Warm-adapted insects developed more quickly, regardless of body size, supporting the “hotter is better” hypothesis that posits that ectotherms have a limited ability to evolutionarily compensate for the depressing effects of low temperatures on rates of biological processes. The remaining unexplained variation in development time likely reflects additional ecological and evolutionary differences among insect species.

Influence of Vectors’ Risk-Spreading Strategies and Environmental Stochasticity on the Epidemiology and Evolution of Vector-Borne Diseases: The Example of Chagas’ Disease

Insects are known to display strategies that spread the risk of encountering unfavorable conditions, thereby decreasing the extinction probability of genetic lineages in unpredictable environments. To what extent these strategies influence the epidemiology and evolution of vector-borne diseases in stochastic environments is largely unknown. In triatomines, the vectors of the parasite Trypanosoma cruzi, the etiological agent of Chagas’ disease, juvenile development time varies between individuals and such variation most likely decreases the extinction risk of vector populations in stochastic environments. We developed a simplified multi-stage vector-borne SI epidemiological model to investigate how vector risk-spreading strategies and environmental stochasticity influence the prevalence and evolution of a parasite. This model is based on available knowledge on triatomine biodemography, but its conceptual outcomes apply, to a certain extent, to other vector-borne diseases. Model comparisons between deterministic and stochastic settings led to the conclusion that environmental stochasticity, vector risk-spreading strategies (in particular an increase in the length and variability of development time) and their interaction have drastic consequences on vector population dynamics, disease prevalence, and the relative short-term evolution of parasite virulence. Our work shows that stochastic environments and associated risk-spreading strategies can increase the prevalence of vector-borne diseases and favor the invasion of more virulent parasite strains on relatively short evolutionary timescales. This study raises new questions and challenges in a context of increasingly unpredictable environmental variations as a result of global climate change and human interventions such as habitat destruction or vector control.

A genetic basis for intraspecific differences in developmental timing?

Heterochrony, altered developmental timing between ancestors and their descendents, has been proposed as a pervasive evolutionary feature and recent analytical approaches have confirmed its existence as an evolutionary pattern. Yet, the mechanistic basis for heterochrony remains unclear and, in particular, whether intraspecific variation in the timing of developmental events generates, or has the potential to generate, future between-species differences. Here we make a key step in linking heterochrony at the inter- and intraspecific level by reporting an association between interindividual variation in both the absolute and relative timing (position within the sequence of developmental events) of key embryonic developmental events and genetic distance for the pond snail, Radix balthica. We report significant differences in the genetic distance of individuals exhibiting different levels of dissimilarity in their absolute and relative timing of developmental events such as spinning activity, eyespot formation, heart ontogeny, and hatching. This relationship between genetic and developmental dissimilarity is consistent with there being a genetic basis for variation in developmental timing and so suggests that intraspecific heterochrony could provide the raw material for natural selection to produce speciation.

Testing the role of phenotypic plasticity for local adaptation: growth and development in time-constrained Rana temporaria populations

Phenotypic plasticity can be important for local adaptation, because it enables individuals to survive in a novel environment until genetic changes have been accumulated by genetic accommodation. By analysing the relationship between development rate and growth rate, it can be determined whether plasticity in life-history traits is caused by changed physiology or behaviour. We extended this to examine whether plasticity had been aiding local adaptation, by investigating whether the plastic response had been fixed in locally adapted populations. Tadpoles from island populations of Rana temporaria, locally adapted to different pool-drying regimes, were monitored in a common garden. Individual differences in development rate were caused by different foraging efficiency. However, developmental plasticity was physiologically mediated by trading off growth against development rate. Surprisingly, plasticity has not aided local adaptation to time-stressed environments, because local adaptation was not caused by genetic assimilation but on selection on the standing genetic variation in development time.

Developmental plasticity as a cohesive evolutionary process between sympatric alternate-year insect cohorts

Many species, particularly insects, pass through a series of distinct phases during their life history, with the developmental timing directed towards appropriate resources. Any factor that creates variation in developmental timing may partition a population into discrete populations-or 'cohorts'. Where there is continued failure to recruit outside the natal cohort then alternate cohorts will have their own internal dynamics, eventually leading to independent demographic and evolutionary trajectories. By contrast, continued variation in development rates within a cohort-cohort splitting-may homogenise otherwise independent demographic units. Using a panel of 14 microsatellite loci, we quantify the genetic signature of apparent demographic isolation between coexisting, but alternate, semivoltine cohorts of the damselfly Coenagrion mercuriale at locations that span its distribution in the UK. We find consistently low levels of genetic divergence between sympatric cohorts of C. mercuriale, indicative of developmental plasticity during the larval stage (unregulated development) whereby some individuals complete their development outside the predominant 2-year (semivoltine) period. Thus, individuals that alter their developmental rate successfully recruit to a different cohort. Despite maintaining contrasting population sizes, gene flow between alternate cohorts broadly is sufficient to place them on a similar evolutionary trajectory and also buffers against loss of genetic diversity. Such flexible larval development permits a response to local conditions and may facilitate response to environmental change.

Optimizing biocontrol using phenological day degree models: the European earwig in pipfruit orchards

1 Phenological day degree models are often used as warning systems for the emergence of arthropod pests in agricultural crops or the occurrence of natural enemies of the pest species. In the present study, we report on a case study of the European earwig Forficula auricularia L., which is an important natural enemy in pipfruit orchards, and describe how such a day degree model can be used to avoid negative effects of crucial orchard management, such as spray applications and soil tillage. A precise timing of these interventions in relation to the phenology of natural enemies will enhance biocontrol. 2 Earwig population dynamics are characterized by single- and double-brood populations, each with specific biological characteristics. 3 A day degree model capable of predicting the phenology of local earwig populations of both population types was developed. The model was checked for accuracy by comparing the first field observation dates of various life stages with predicted values using temperature data from the nearest weather station. In addition, variation in development time was assessed using field data. 4 The model was able to make predictions on a global scale. Although single- and double-brood populations differ in phenology, the predictions of first appearance dates were similar. Variation in development time showed that single-brood populations were more synchronized. 5 Our phenological model provides an accurate tool for predicting and simulating earwig population dynamics, as well as for enhancing the biocontrol of pests in pipfruit orchards.

Independence of genetic variation between circadian rhythm and development time in the seed beetle, Callosobruchus chinensis

A positive genetic correlation between periods of circadian rhythm and developmental time supports the hypothesis that circadian clocks are implicated in the timing of development. Empirical evidence for this genetic correlation in insects has been documented in two fly species. In contrast, here we show that there is no evidence of genetic correlation between circadian rhythm and development time in the adzuki bean beetle, Callosobruchus chinensis. This species has variation that is explained by a major gene in the expression and period length of circadian rhythm between strains. In this study, we found genetic variation in development time between the strains. The development time was not covaried with either the incidence or the period length of circadian rhythm among the strains. Crosses between strains suggest that development time is controlled by a polygene. In the F2 individuals from the crosses, the circadian rhythm is attributable to allelic variation in the major gene. Across the F2 individuals, development time was not correlated with either the expression or the period length of circadian rhythm. Thus, we found no effects of major genes responsible for variation in the circadian rhythm on development time in C. chinensis. Our findings collectively give no support to the hypothesis that the circadian clock is involved in the regulation of development time in this species.

Simulation model of the red flour beetle in flour mills.

Simulation model of the red flour beetle in flour mills.

Stage-Specific Effects of Candidate Heterochronic Genes on Variation in Developmental Time along an Altitudinal Cline of Drosophila melanogaster

BackgroundPreviously, we have shown there is clinal variation for egg-to-adult developmental time along geographic gradients in Drosophila melanogaster. Further, we also have identified mutations in genes involved in metabolic and neurogenic pathways that affect development time (heterochronic genes). However, we do not know whether these loci affect variation in developmental time in natural populations.Methodology/Principal FindingsHere, we constructed second chromosome substitution lines from natural populations of Drosophila melanogaster from an altitudinal cline, and measured egg-adult development time for each line. We found not only a large amount of genetic variation for developmental time, but also positive associations of the development time with thermal amplitude and altitude. We performed genetic complementation tests using substitution lines with the longest and shortest developmental times and heterochronic mutations. We identified segregating variation for neurogenic and metabolic genes that largely affected the duration of the larval stages but had no impact on the timing of metamorphosis.Conclusions/SignificanceAltitudinal clinal variation in developmental time for natural chromosome substitution lines provides a unique opportunity to dissect the response of heterochronic genes to environmental gradients. Ontogenetic stage-specific variation in invected, mastermind, cricklet and CG14591 may affect natural variation in development time and thermal evolution.

Developmental variability and stability in continuous-time host–parasitoid models

Insect host–parasitoid systems are often modeled using delay-differential equations, with a fixed development time for the juvenile host and parasitoid stages. We explore here the effects of distributed development on the stability of these systems, for a random parasitism model incorporating an invulnerable host stage, and a negative binomial model that displays generation cycles. A shifted gamma distribution was used to model the distribution of development time for both host and parasitoid stages, using the range of parameter values suggested by a literature survey. For the random parasitism model, the addition of biologically plausible levels of developmental variability could potentially double the area of stable parameter space beyond that generated by the invulnerable host stage. Only variability in host development time was stabilizing in this model. For the negative binomial model, development variability reduced the likelihood of generation cycles, and variability in host and parasitoid was equally stabilizing. One source of stability in these models may be aggregation of risk, because hosts with varying development times have different vulnerabilities. High levels of variability in development time occur in many insects and so could be a common source of stability in host–parasitoid systems.

Mating behaviour, life history and adaptation to insecticides determine species exclusion between whiteflies

1. Negative interspecific interactions, such as resource competition or reproductive interference, can lead to the displacement of species (species exclusion). 2. Here, we investigated the effect of life history, mating behaviour and adaptation to insecticides on species exclusion between cryptic whitefly species that make up the Bemisia tabaci species complex. We conducted population cage experiments independently in China, Australia, the United States and Israel to observe patterns of species exclusion between an invasive species commonly referred to as the B biotype and three other species commonly known as biotypes ZHJ1, AN and Q. 3. Although experimental conditions and species varied between regions, we were able to predict the observed patterns of exclusion in each region using a stochastic model that incorporated data on development time, mating behaviour and resistance to insecticides. 4. Between-species variation in mating behaviour was a more significant factor affecting species exclusion than variation in development time. Specifically, the ability of B to copulate more effectively than other species resulted in a faster rate of population increase for B, as well as a reduced rate of population growth for other species, leading to species exclusion. The greater ability of B to evolve resistance to insecticides also contributed to exclusion of other species in some cases. 5. Results indicate that an integrative analysis of the consequences of variation in life-history traits, mating behaviours and adaption to insecticides could provide a robust framework for predicting species exclusion following whitefly invasions.