Timing Of Diapause Induction Research Articles

Different photoperiodic responses in diapause induction can promote the maintenance of genetic diversity via the storage effect in Daphnia pulex.

Understanding mechanisms that promote the maintenance of biodiversity (genetic and species diversity) has been a central topic in evolution and ecology. Previous studies have revealed that diapause can contribute to coexistence of competing genotypes or species in fluctuating environments via the storage effect. However, they tended to focus on differences in reproductive success (e.g. seed yield) and diapause termination (e.g. germination) timing. Here we tested whether different photoperiodic responses in diapause induction can promote coexistence of two parthenogenetic (asexual) genotypes of Daphnia pulex in Lake Fukami-ike, Japan. Through laboratory experiments, we confirmed that short day length and low food availability induced the production of diapausing eggs. Furthermore, we found that one genotype tended to produce diapausing eggs in broader environmental conditions than the other. Terminating parthenogenetic reproduction earlier decreases total clonal production, but the early diapausing genotype becomes advantageous by assuring reproduction in 'short' years where winter arrival is earlier than usual. Empirically parameterized theoretical analyses suggested that different photoperiodic responses can promote coexistence via the storage effect with fluctuations of the growing season length. Therefore, timing of diapause induction may be as important as diapause termination timing for promoting the maintenance of genetic diversity in fluctuating environments.

Partial reuse of circadian clock genes along parallel clines of diapause in two moth species.

Understanding the molecular basis of repeated evolution improves our ability to predict evolution across the tree of life. Only since the last decade has high-throughput sequencing enabled comparative genome scans to thoroughly examine the repeatability of genetic changes driving repeated phenotypic evolution. The Asian corn borer (ACB), Ostrinia furnacalis (Guenée), and the European corn borer (ECB), Ostrinia nubilalis (Hübner), are two closely related moths displaying repeatable phenological adaptation to a wide range of climates on two separate continents, largely manifesting as changes in the timing of diapause induction and termination across latitude. Candidate genes underlying diapause variation in North American ECB have been previously identified. Here, we sampled seven ACB populations across 23 degrees of latitude in China to elucidate the genetic basis of diapause variation and evolutionary mechanisms driving parallel clinal responses in the two species. Using pooled whole-genome sequencing (Pool-seq) data, population genomic analyses revealed hundreds of single nucleotide polymorphisms (SNP) whose allele frequencies covaried with mean diapause phenotypes along the cline. Genes involved in circadian rhythm were over-represented among candidate genes with strong signatures of spatially varying selection. Only one of two circadian clock genes associated with diapause evolution in ECB showed evidence of reuse in ACB (period [per]), but per alleles were not shared between species nor with their outgroup, implicating independent mutational paths. Nonetheless, evidence of adaptive introgression was discovered at putative diapause loci located elsewhere in the genome, suggesting that de novo mutations and introgression might both underlie the repeated phenological evolution.

Do genetic differences in growth thermal reaction norms maintain genetic variation in timing of diapause induction?

AbstractAn optimal timing for diapause induction through the sexual production of dormant propagules is expected in organisms with temporary populations. Yet, empirical studies often find high within‐population genetic variation in the sexual production of such propagules, suggesting that this is a common feature of such organisms.Here, we hypothesize that genetic variation in the propensity to produce dormant propagules,Pd, is maintained by a genotype‐by‐environment interaction in clonal reproductive rates, where fast‐growing genotypes within an environment should delay diapause relative to slow‐growing genotypes. From this, we derive two predictions. First, if reaction norms of clonal reproduction cross between two environments, the genetic correlation ofPdbetween these environments should be negative. Second, the correlation between plasticity values of clonal reproduction andPdshould be negative.We tested these predictions by quantifying ephippia production in genotypes of a population of the facultative sexual cladoceranDaphnia magnaat two temperatures. The population biomass at the onset of ephippia production was used as a measure ofPd, whereas juvenile somatic growth rate was used as a proxy for clonal reproductive rate. Plasticity for both measurements was derived from thermal reaction norms.Our results did not support either prediction, as neither the genetic correlation ofPdbetween environments, nor the correlation between plasticity values of growth andPdwere found to be significant.Our results suggest that genetic variation in the timing of diapause is not maintained by genetic differences in thermal clonal reproduction reaction norms. We propose as an alternative hypothesis that if there is variation across years in how the environment deteriorates over a season, fluctuating selection may favor genotypes with differentPdbetween years.

Geographic variation of temperature effects on initial colony development of Lasius japonicus (Hymenoptera: Formicidae)

For Lasius japonicus Santschi (Hymenoptera: Formicidae), a common ant species in Japan, diapause induction is temperature dependent. To elucidate the geographic variation of its temperature dependence, new L. japonicus queens were collected immediately after nuptial flight from four sites at different latitudes: Kitami (44.1°N), Hakodate (41.8°N), Shizuku-ishi (39.7°N), and Okayama (34.7°N). The collected queens were reared for 100 days at four constant-temperature conditions (25 °C, 20 °C, 17.5 °C, and 15 °C) under a 12L:12D photoperiod. The queens began founding colonies immediately in all conditions. For all temperature conditions, daily change patterns of the average numbers of eggs, larvae, and pupae were similar among the Hakodate, Shizuku-ishi, and Okayama populations, but the development patterns of the Kitami colonies differed from those of the other three sites. Low temperatures strongly suppressed colony development of the Kitami population; development was weak even at moderate temperatures. For new queens of L. japonicus, solitary overwintering without rearing larvae is regarded as serving an important role in successful colony foundation under cool climate conditions. Results reported herein suggest that local temperatures exert important selective pressure on the timing of diapause induction and on colony development in northern populations.

Seasonal adaptations of the scarce silver-lines Bena bicolorana (Fuessly, 1775) (Lepidoptera, Noctuidae)

The influence of photoperiod and temperature on the growth and development of the scarce silver-lines Bena bicolorana (Fuessly, 1775) (Lepidoptera, Noctuidae) was studied in Belgorod Province, Russia (50°N, 36°E). At temperatures of 21 and 24°C, all photoperiodic regimes with 12 to 17 h of light per day induced diapause in the IV instar larvae. At 24°C, under long-day conditions with a photophase of 18 h, both diapausing and nondiapausing (i.e., directly developing) IV instar larvae were recorded in almost equal proportions; this photoperiodic regime may thus be considered as the threshold one. Diapause induction in B. bicolorana was associated with the larvae changing color from light green to brick-red. The larval growth rates, their weight dynamics, and timing of diapause induction are under photoperiodic control. Thus, seasonal development of B. bicolorana is controlled by two photoperiodic responses: the qualitative one that controls larval diapause induction, and the quantitative one that regulates larval growth parameters before diapause induction. In Belgorod Province B. bicolorana annually produces only one generation, what agrees well with the parameters of both of its photoperiodic responses. The results of the experimental eco-physiological studies support the separation of the monotypic genus Bena because it includes the only species in the subfamily Chloephorinae (B. bicolorana) that overwinters at the larval stage.

Intra‐population genetic variation in diapause incidence of adult‐diapausing Tetranychus pueraricola (Acari: Tetranychidae)

Diapause is an important seasonal adaptation for arthropods in temperate regions. Recent global warming has had a profound effect on the timing of diapause induction, but the potential for evolutionary changes in diapause attributes remains largely unknown because of a scarcity of information about genetic architecture in these traits. Genetic variation in diapause incidence within a population and the genetic correlation with different environmental conditions are both important for predicting evolutionary responses to climatic changes. The main aim of this study was to determine these parameters at temperatures representative of the winter season (stationary 18–20 °C) by using 12 isofemale lines established from females of a single population of the adult‐diapausing spider mite Tetranychus pueraricola (Acari: Tetranychidae). To compare the response between field and laboratory, their ancestral phenotypes were randomly chosen from diapausing (eight) or non‐diapausing (four) females. Diapause incidence was investigated at 18, 19, and 20 °C under LD 10:14 h conditions with two to five replicates for each strain. At 18 °C, more than 90% of the females entered diapause, and the genetic variation among strains (intraclass correlation coefficient; ICC) was relatively small (44%), whereas highly variable diapause incidences were observed for the warmer conditions (both 87% ICC). The correlation between temperatures was as high as 0.79 between 19 and 20 °C, whereas the correlation estimates between 18 and either 19 or 20 °C were still positive, but not significant. In addition, the analyses demonstrated the existence of variation in the entire response curves (significant genotype × environment interaction). These results demonstrate that significant genetic variation in response curves is maintained in this population, and accordingly this population has a capacity to respond to climatic changes. Crossing reaction curves across temperatures may prevent the fixation of a single optimal response curve, and maintain genetic variation at each temperature.

Timing of diapause induction and overwintering success in the cotton bollworm Helicoverpa armigera (Hb.) (Lepidoptera: Noctuidae) under outdoor conditions in temperate Japan

The timing of diapause induction and overwintering success in the cotton bollworm Helicoverpa armigera were studied outdoors in Chiba (35°N, 140°E) and Kyoto (35°N, 135°E) prefectures, Japan, using local populations collected from Chiba and Mie (34°N, 136°E) Prefectures, respectively. For comparison, a similar experiment was performed in Chiba using a closely related species, H. assulta. Diapause induction in H. armigera was stimulated by low temperatures in autumn, and the incidence of pupal diapause increased sharply with little change in photoperiod. In Kyoto, pupae of H. armigera overwintered successfully in a state of diapause. However, larvae that had hatched from eggs deposited in late autumn suffered high mortality, presumably from the cold; therefore, the pattern of temperature change in autumn credibly affects overwintering success in H. armigera. In contrast, a considerable number of H. assulta pupae entered diapause well before autumn, even though those individuals had hatched from eggs deposited during the mid-summer. Thus, H. assulta appeared to prepare for overwintering earlier and more successfully than did H. armigera in this temperate zone. Differences in diapause induction between the sexes revealed in laboratory experiments with H. armigera were not detected under outdoor conditions.

Timing of diapause induction and its life‐history consequences in Nezara viridula: is it costly to expand the distribution range?

Abstract. 1. From the early 1960s to 2000 Nezara viridula (Heteroptera: Pentatomidae) expanded its range northwards in Japan and reached Osaka following climate warming recorded in the region.2. The timing of diapause induction and its effect on life‐history traits were studied under quasi‐natural conditions in Osaka. Egg masses were placed outdoors in six series in July–November 1999. Developmental events were monitored until September 2000.3. Adult diapause was induced in September–October in agreement with the photoperiodic response obtained under laboratory conditions. Induction of diapause in early October ensured the highest winter survival. Nymphs that hatched after late September died by December–April showing that the species cannot survive winter in the nymphal stage.4. Life‐history traits varied between the early (non‐diapause reproduction) and late (post‐diapause reproduction) series. Thus, non‐diapause females produced significantly fewer egg masses than did females that reproduced only after diapause. The timing of diapause induction strongly affected overwintering success and post‐diapause performance: females that became adults and entered diapause in October lived longer, had a longer period of oviposition, and produced more eggs in larger egg masses than females that attained adulthood and entered diapause in September.5. Females from the early series reproduced until late November, although progeny from the late September eggs were destined to die during the winter. Pre‐winter reproduction of adults that emerged in mid‐September or later was a result of the imperfect timing of diapause induction. It is an ineffective allocation of resources and may be considered the ecological cost of range expansion.6. To establish in the region, N. viridula will probably evolve a lengthening of the critical photoperiod of the diapause induction response. This will allow the species to enter diapause earlier and, thus, avoid maladaptive late‐autumn reproduction but, perhaps, increase the cost of diapause because of a possible adverse impact of pre‐winter high temperature conditions on overwintering.

Timing of diapause induction outside the natural distribution range of a species: an outdoor experiment with the bean bug Riptortus clavatus

AbstractThe phytophagous bug Riptortus clavatus (Thunberg) (Heteroptera: Alydidae) produces two or three generations per year in Central Japan and overwinters in the adult stage. In bugs from the Kyoto population (35°00′ N, 135°45′ E), we studied (1) the effects of day‐length on the nymphal and preoviposition periods under constant photoperiod at 20.5 °C, and (2) photoperiodic induction of adult diapause at 20.5 °C and under a combination of constant photoperiod and natural daily rhythm of temperature in the forest‐steppe zone of Russia (50°38′ N, 35°58′ E). Then, we examined (3) the timing of diapause induction under quasi‐natural conditions in the same region, far outside the species' natural geographical range. At 20.5 °C, the nymphal period in both males and females was significantly longer under regimes with shorter photophases than under those with longer photophases. The preoviposition period in females was significantly longer under the near‐critical long‐day regime L14:D10 than under typical long‐day regimes (L15:D9, L16:D8, and L17:D7). The critical day‐length for diapause induction was shorter under conditions of natural daily rhythm of temperature than those reported at constant 20, 25, and 30 °C. Under quasi‐natural conditions in the forest‐steppe zone, R. clavatus entered diapause in September, much later than the local populations of true bugs studied to date. This experiment showed that R. clavatus was maladapted to new environmental conditions: diapause was induced too late with the result that all or most nymphs hatched in late August or early September will die.

Fitness Functions for Alternative Developmental Pathways in the Timing of Diapause Induction

We analyze five commonly occurring ontogenetic relationships between the sensitive period (SP) for diapause induction, during which environmental cues are assessed and the decision is made whether to diapause, and the diapause stage (DS), during which normal development ceases and diapause characteristics prevail. One relationship (case 1), in which both the SP and DS occur in the juvenile stages of the same generation, has previously been analyzed in detail. Here we concentrate on the remaining four developmental pathways. In case 2a, the DS is the adult preceded by a determinate SP. Since a determinate SP has a fixed end before reproduction, adults are committed to reproduction or to diapause before reproducing. In case 2b, the DS is the adult preceded by an indeterminate SP, which has no fixed end and extends into the reproductive adult stage, allowing an adult to reproduce before entering diapause. The parental generation in case 3a determines the diapausing fate of a preadult stage in the next genera...

Estimating the ends of the sensitive period for photoperiodically induced diapause in arthropods

A new method is proposed and tested for estimating the beginning and end of the sensitive period for the photoperiodic induction of diapause (a type of dormancy) in arthropods. The method incorporates three experiments already commonly used to study photoperiodism: (1) an experiment in which samples of individuals are transferred at successively older ages from a diapause inducing short day length to a diapause averting long day length, (2) an experiment in which samples are transferred at successively older ages in the opposite direction from long to short day conditions, and (3) an experiment to determine the number of short days required to induce diapause, the required day number. Using the Mexican bean beetle ( Epilachna varivestis Mulsant), which has an adult diapause, the new method estimates that this beetle's sensitive period at 25°C begins approximately on day 9 for males and on day 10 for females corresponding to the beginning and early second instar, respectively, and ends on day 21 for both sexes corresponding to the start of the pupal stage. The observation that the sensitive period is 1 day longer for males resolves the otherwise inconsistent findings that the mean required day number is 1 day greater for males but the critical photoperiod is the same for both sexes. To assess the responses of the beetles to the experiments, they were dissected on day 4 after adult eclosion and classified according to their level of gonadal development. Four classes were recognized in females and 3 in males yielding 3 and 2 thresholds, respectively, instead of the usual single threshold separating the diapause and nondiapause classes. Estimates of the ends of the sensitive period using the different thresholds were consistent. Obtaining reliable estimates of the ends of the sensitive period is an important step toward the goal of using the physiological model of diapause induction based on the required day number-sensitive period interaction to address ecological and evolutionary questions concerning the timing of diapause induction.