THE ROLES OF FLUCTUATING SELECTION AND LONG-TERM DIAPAUSE IN MICROEVOLUTION OF DIAPAUSE TIMING IN A FRESHWATER COPEPOD

Direct observations of selection response in natural, unmanipulated populations in the wild are rare. Those that exist have resulted from major changes in environment during an ongoing study. Selection response should be more common and more readily observable in short-lived organisms where the direction of selection changes from year to year. We examined how the interaction of fluctuating selection, and emergence from long-term diapause, caused ongoing microevolutionary change over eight years in an important life-history trait (diapause timing) in the freshwater calanoid copepod Diaptomus sanguineus. Emergence from long-term diapause releases into the population lineages that did not experience the most recent bout of selection, thereby promoting the maintenance of the heritable trait variation that allows continual selection response. A mechanistic selection model was created on the basis of field and laboratory studies to predict how interannual variations in predation intensity generate year-to-year changes in mean diapause timing and in net reproductive success for alternate trait values. The predicted selection response and the estimated effect of emergence from diapause were both significantly correlated with observed changes in trait mean. A linear model combining selection response and emergence from diapause explained 59% of the variance in year-to-year changes in trait mean. According to this model, strong selection occurred in about half of the years studied, and the average annual contributions to changes in trait mean from selection and emergence were roughly equal. Thus, both fluctuating natural selection and emergence from prolonged diapause affect the expression of diapause timing by D. sanguineus. Fluctuating selection is ubiquitous in nature and may provide opportunities in other populations to witness ongoing natural selection without directional trends in mean phenotype.     

Response of diapausing eggs hatching to changes in temperature and the presence of fish kairomones

It has been hypothesized that the production of diapausing eggs in Daphnia can be induced by fish kairomones. A population of Daphnia could survive severe predation using this predator avoidance strategy. However, in changing environments, diapausing eggs experience various temperature conditions, and hatchlings at emergence may be exposed to the same predation risks as their mothers. Therefore, staying in diapause or an immediate response upon hatching to available environmental information could be important for hatchling survival. For this study, we investigated the impact of water temperature (10, 15, 20, and 25°C) in the presence and absence of fish kairomones (Lepomis macrochirus) on the hatching success of resting eggs (D. galeata). Results show that no diapausing eggs hatched at the lowest temperature (10°C), and the highest hatch percentage occurred at 15°C. Although higher water temperatures reduced hatching success, diapausing eggs hatched more quickly. The number of hatchlings was significantly higher after exposure to fish kairomones, and this was more noticeable at higher temperatures (20 and 25°C). The present results suggest that the diapausing eggs were produced as a predator avoidance strategy in Daphnia; however, the presence of fish works as a positive signal to increase hatchlings when the diapausing stage is terminated.     

Does the Number of Diapausing Eggs Laid on Bark Affect the Population Dynamics of the Spider Mite Panonychus mori?

We studied the relationship between number of diapausing eggs produced by the spider mite Panonychus mori and the subsequent population trend for a period of 3 years. Panonychus mori showed a single population density peak on its host plant moonseed, Cocculus trilobus. The position and height of this peak were correlated with the density of diapausing eggs around the moonseed leaf buds produced the winter before. In 1994 the density of diapausing eggs measured in February was 4.3/bud, which was 6–14 times higher than the density of diapausing eggs for the same period in 1995 (0.3/bud) and 1996 (0.7/bud). The subsequent population density peak in 1994 occurred in mid June and was about 2.5 times higher than the peaks in 1995 and 1996, which both occurred early September. Thus, the present study showed a positive correlation between the density of diapausing eggs on the host plant and the start and the extend of the population increase the next growing season. Predators associated with the spider mite population were phytoseiid mites, especially Amblyseius eharai was well synchronized with the spider mite density in 1994. Field observations revealed that P. mori produced diapausing eggs in response to short photoperiod in early October each year, which corresponded with the timing predicted by the critical photoperiod around 13 h at 18°C, as assessed in laboratory trials. Diapause ended by early April when egg hatchability attained about 50% and eggs took 9 days to hatch at 25°C and a 16L:8D photoperiod. Hatching in early April was twice faster than in late February.     

Structure, development and induction of a new diapause stage in rotifers

1. This study shows that females of Synchaeta pectinata Ehrenberg can produce two morphologically and physiologically distinct kinds of amictic eggs that develop parthenogenetically into females. One kind, until now the only one known in monogonont rotifers, is a thin-shelled (about 1.4 μm) subitaneous egg that develops without arrest. The other kind is a thick-shelled (about 9 μm) egg that enters obligatory diapause after 1–3 cleavage divisions before resuming development. The thicker shell of the diapausing egg is due to an expansion of the outer sublayer of the single-layered shell. 2. The mean duration of the diapause at 19 °C (L : D 16 : 8) is about 14 days. This diapause is not broken by low temperature (5 °C), and it is not greatly extended by storage at low temperature (5 °C). 3. Diapausing eggs are induced immediately after a brief starvation period, and seem to be produced at no additional energetic cost. However, a population producing a high proportion of diapausing eggs has a much reduced reproductive potential. 4. Production of diapausing amictic eggs may be a strategy to increase the ability of clones to survive food limitation. 5. Diapausing amictic eggs differ markedly from fertilized resting eggs produced following bisexual reproduction during favourable conditions.     

Predator-induced diapause in Daphnia magna may require two chemical cues

The production of diapausing eggs by Daphnia magna stimulated by fish exudates can be explained as an anti-predator defence ensuring genome protection in periods of high risk from fish predation. The combined effects on the induction of D. magna diapause of an “alarm” chemical originating from injured conspecific prey and fish kairomones were tested. The results of the experiment showed that the cues when present together promote both the production of ephippial eggs and male formation, indicating their role in the synchronization of the entire mode of Daphnia sexual reproduction. Ephippial eggs were only produced in the presence of both fish kairomone and conspecific alarm chemicals, while male offspring occurred in the treatments where both, one or none of the cues were present. However, production of males was the highest when both cues were provided. D. magna responded similarly to the tested cues whether or not the hypothetical alarm substance associated with predator odour came from Daphnia specimens actually eaten by fish or from crushed conspecific individuals. However, chemicals from crushed chironomid larvae combined with fish kairomones did not induce a similar response in D. magna. The relative advantage of utilization of alarm cues or predator kairomones in the induction of defence responses in prey organisms is discussed. Received: 8 June 1998 / Accepted: 11 January 1999     

Induction of larval diapause in the blowfly, Calliphora vicina R.-D. (Diptera, Calliphoridae) under field and laboratory conditions

Field experiments conducted in the environs of St. Petersburg (Russia) with a local population of Calliphora vicina showed that induction of larval diapause under natural conditions was significantly dependent on day lengths and temperature. The maternal photoperiodic response had a distinct threshold: the first diapausing larvae hatched from the eggs laid in the middle of August when the day length was 16 h; at shorter photoperiods, the fraction of diapausing larvae depended only on temperature. At the mean temperature of 16°C, larval diapause was rarely recorded; at 12–13°C, about 50% of the larvae entered diapause; at 7–9°C, nearly all the larvae entered diapause. These results of the field experiments agree well with the parameters of photoperiodic and thermal responses studied in the laboratory at constant temperatures and photoperiods.     

Fish as vectors in the dispersal of Bythotrephes cederstroemi: diapausing eggs survive passage through the gut

• 1 Bythotrephes cederstroemi (Crustacea: Onychopoda: Cercopagidae) is an introduced invertebrate predator currently spreading through the Laurentian Great Lakes region of North America. We examined a previously unsuspected way in which B. cederstroemi may be dispersed by fish by their consumption of diapausing eggs.
• 2 Ninety‐four percentage of the mature B. cederstroemi diapausing eggs consumed by fish were egested apparently intact. This proportion is considerably above previous estimates for the ephippial eggs of Daphnia. The hatching success of diapausing eggs was compared among four categories: (a) eggs released naturally by B. cederstroemi (control, 73% hatched) (b) eggs released during ‘stressful confinement’ (46% hatched) (c) eggs dissected from dead females (13% hatched) and (d) eggs recovered from faecal pellets following consumption by fish (viable gut passage experiment, 41% hatched).
• 3 Samples of small fish and B. cederstroemi were collected simultaneously. Examination of gut contents revealed that fish contained B. cederstroemi diapausing eggs and that B. cederstroemi bearing resting eggs were consumed selectively over those without eggs. Moreover, fish selected B. cederstroemi bearing mature rather than immature diapausing eggs.
• 4 The fact that diapausing eggs survive gut passage is important for the dispersal of B. cederstroemi. Fish often move between the pelagic and littoral zones of lakes and may thus disperse diapausing eggs widely. Fish may also move between lakes connected by river systems and can be caught and passively dispersed by anglers or piscivorous birds. Our results demonstrate the potential for fish to act as vectors in the spread of B. cederstroemi.

     

Experimental evolution of bet hedging in rotifer diapause traits as a response to environmental unpredictability

The adaptive response of organisms to unpredictable environments is increasingly recognized as a central topic in fundamental and applied evolutionary ecology. Selection due to environmental unpredictability can act on multiple traits of an organism's life cycle to reduce the impact of high environmental variance. The aim of this research was to study how unpredictability selects for diapause traits: 1) the timing of sex (a proxy of the timing of diapausing egg production), and 2) the diapausing egg hatching fraction (a proxy of diapause duration). We used an experimental evolution approach with the facultative sexual rotifer Brachionus plicatilis. Laboratory populations experiencing two contrasting regimes of environmental fluctuation (predictable versus unpredictable) evolved divergently over a short time span (< 77 days). The populations under the unpredictable regime showed an earlier initiation of sexual reproduction and a lower hatching fraction of diapausing eggs than populations under the predictable regime. These findings demonstrate empirically the existence of bet‐hedging strategies in B. plicatilis regarding both traits, consistent with theoretical predictions of bet‐hedging evolution under conditions of unpredictable environmental variance. Given that scenarios of increased environmental variability are expected to occur in the near future, a comprehensive understanding of the role of bet‐hedging strategies is necessary for predicting population responses to environmental change.     

Role of temperature in diapause response to fish kairomones in crustacean Daphnia

The effect of non-lethal thermal conditions on the diapause response to a simulated threat of fish predation was tested in the freshwater planktonic crustacean Daphnia magna.From an early developmental stage, female Daphnia were either exposed or not exposed to fish kairomones that notified of the threat of fish predation at the benign growth temperatures of 18, 22 or 26 °C. The proportion of females switching from the production of subitaneous to diapausing eggs and their rate of reproduction were recorded.Besides the faster development and more intense reproduction observed at higher temperatures, a smaller proportion of the females formed protective, diapausing eggs when exposed to fish kairomones than was the case in colder conditions. The production of diapausing eggs was not observed when the threat of fish predation was absent. These results indicate an interactive effect of fish kairomones and thermal conditions on diapause induction in D. magna.We interpret these findings in the context of strategies for the maximisation of reproductive success. The production of well protected diapausing eggs (which assures low yet stable gains under diverse thermal conditions) may be a more beneficial life history strategy at lower temperatures, where the chances of survival of active individuals until maturation and successful reproduction are low. Higher temperatures permit faster maturation and more intensive reproduction that may surpass numerical losses of active descendants due to predation, making diapause a less rewarding option.     

Population differences in the timing of diapause: a test of hypotheses

Summary The reproductive phenology of the freshwater copepod Diaptomus sanguineus differs markedly between populations residing in two Rhode Island ponds. In a permanent pond the population switches abruptly from making subitaneous (immediately hatching) eggs to diapausing eggs at the end of March each year. In contrast, a temporary pond population switches egg types in May, returns to production of subitaneous eggs in June, and concludes the reproductive season by making diapausing eggs in July. An ESS model suggests that the pattern of diapause expected of a copepod population is a function of annual variation in the onset of harsh conditions (catastrophe date). When variation is relatively low, the superior strategy is for diapause to begin a constant period before the mean catastrophe date. When variation is high, females should make first subitaneous eggs and then diapausing eggs irrespective of the expected catastrophe date. With discrete generations, such a population would alternate between egg types. In the permanent pond, variation of catastrophe date the spring onset of planktivory by sunfish is low, whereas in the temporary pond variation of the catastrophe (pond drying) is high. The model predicts well the phenology of the two copepod populations.In the research reported here, we tested the hypothesis that copepods from the permanent pond, which switch to diapause at the same time every year, are cued by the environment to begin diapause (i.e. by photoperiod, temperature, or both), whereas those from the temporary pond make both egg types regardless of environmental conditions. In opposition to our hypothesis, experimental results indicate that diapause in both populations is cued by the environment. The distinct reproductive phenologies documented in the two populations apparently result from the copepods responding to different environmental cues, rather than one being responsive to the environment while the other is not.     

Phenological adaptations of a colonizing insect: The southwestern corn borer,Diatraea grandiosella

Summary The developmental rate, critical photoperiod, and diapause intensity were determined for three populations of the southwestern corn borer, Diatraea grandiosella, from Missouri, Mississippi and Kansas. Mississippi larvae grew at the highest rate and Missouri larvae grew at the lowest rate. The zero developmental temperatures (°C) for the Missouri population were estimated from regression lines as follows: 10.5° (eggs), 10.8° (diapausing larvae), 13.3° (non-diapausing larvae) and 11.4° (pupae). The required heat units were: 85° (eggs), 588° (diapausing larvae), 333° (non-diapausing larvae) and 149° days (pupae). However, the observed low temperature limit for larval growth under constant temperature regimes was approximately 17°C.The critical day lengths for diapause induction observed at 25°C were: 15 h 11 min (Missouri); 15 h 20 min (Mississippi); and 15 h 22 min (Kansas). The photoperiodic response of the Mississippi larvae was more or less retained at 30°C, whereas the response of the Missouri larvae was completely suppressed at this temperature. Diapause was most easily terminated in the Kansas larvae. The most intense diapause was observed in the Mississippi larvae.Model seasonal life cycles of the three geographic populations were constructed using photothermograms. Although the models showed good agreement with the field situation for the Missouri and the Kansas populations, some unknown factor(s) remains to account for an extremely long critical photoperiod in the Mississippi population.Contribution from the Missouri Agricultural Experiment Station, as journal series no. 9001     

Diapause and implications for control of Penthaleus species and Halotydeus destructor (Acari: Penthaleidae) in southeastern Australia

Blue oat mites, Penthaleus spp., and redlegged earth mites, Halotydeus destructor (Tucker) are major winter pests of a variety of crops and pastures. In southern Australia earth mites exhibit a facultative egg diapause to survive unfavorable summer conditions. The initiation of diapause egg production in earth mites was investigated using field and shade-house experiments. Species differed in their timing of diapause. H. destructor mainly produced diapausing eggs towards the end of the active mite season in spring, although small numbers were also produced in winter. In contrast, Penthaleus major (Dugés) produced diapause eggs almost immediately after emergence in autumn and continued producing these eggs throughout the season. Penthaleus falcatus (Qin and Halliday) also produced diapause eggs in early winter, although the first appearance of these eggs was slightly later in the season than for P. major. The diapause response of an undescribed species was also somewhat later than in P. major and P. falcatus, but earlier than in H. destructor. Electrophoresis of P. major samples indicated that clones of this parthenogenic species may differ in their timing of diapause egg production, providing another potential selective factor contributing to the maintenance of clonal diversity within this group. The results highlight the importance of determining species composition when devising control strategies for earth mite outbreaks.     

Local variation in overwintering stages ofPanonychus akitanus Ehara (Acarina: Tetranychidae)

The overwintering behaviour ofPanonychus akitanus Ehara was compared in a population (Sapporo) overwintering as the egg and the adult female and in a population (Tomakomai) overwintering in the egg stage only. In both populations, winter eggs were larger in size and darker in colour than summer eggs, and females laying winter eggs showed clear differences in body colour and behaviour from summer females. Both populations produced winter eggs in response to short photoperiods, and the critical photoperiod was between 13.0 and 13.5 h in the Sapporo population and between 13.5 and 14.0 h in the Tomakomai population. The hatchability of winter eggs of the Sapporo population collected from the field began to increase in November, and that of the Tomakomai population in December. In the Sapporo population, a 40-day or more exposure to 5°C promoted hatching of winter eggs, and a 50-day exposure of females which had previously laid some winter eggs to 5°C induced the production of summer eggs. Females of the Sapporo population laid winter eggs in autumn, and then themselves overwintered as well, and produced summer eggs in the following spring. These females were called winter-habit females.The winter eggs of both populations were diapausing. However, the winter-habit females of the Sapporo population were not reproductively inactive and their condition of diapause was not certain. The ecological significance of the winter-habit females in the Sapporo population is discussed.     

Population differences in the timing of diapause: adaptation in a spatially heterogeneous environment

Summary Populations of the planktonic copepod, Diaptomus sanguineus, live in permanent and temporary freshwater ponds in Rhode Island. All ponds in which they occur become uninhabitable at some time during the year, but the nature and timing of the harsh period varies both spatially and temporally. Females produce discrete clutches either of subitaneous eggs which hatch immediately or of diapausing eggs which hatch the following season. The two egg types show distinct chorion morphologies under transmission electron microscopy. In permanent ponds the copepods start making diapausing eggs in March, one month before rising water temperatures induce planktivorous sunfish to become active. In temporary ponds diapausing eggs are produced, in a complex pattern from May to July, before the water disappears in late summer or early fall.We investigated the spatial scale at which D. sanguineus is adapted to this complex environment. In a reciprocal transfer experiment between temporary and permanent bodies of water, female copepods placed in new ponds made subies of water, female copepods placed in new ponds made subitaneous and diapausing eggs in the same sequence as control females retained in their home ponds. The copepod populations enter diapause at times appropriate for the local habitat conditions they experience, but inappropriate for other, nearby ponds. Transplanted females were unable to sense a change in pond type or to adjust egg production accordingly. We conclude that D. sanguineus populations are adapted to the specific conditions of isolated ponds rather than to a broader geographical region containing several pond types.     

Diapause dynamics of two diaptomid copepod species in a large lake

Skistodiaptomus oregonensis and Leptodiaptomus minutus produce diapausing eggs in a large lake, Oneida Lake, in New York State. The timing of the switch from production of subitaneous (immediately hatching) eggs to diapausing eggs for both species is in October. This timing is consistent with a pattern, reviewed here, for other populations of diaptomid copepods: populations living in large lakes tend to begin production of diapausing eggs later in the season than those living in small lakes. Populations living in temporary ponds tend to switch still earlier in the season. All populations reviewed here live in the north temperate zone. The sediments of Oneida Lake contain densities of diaptomid diapausing eggs on the order of 10⁵ m^–2 per cm below the sediment surface down to 5 cm. Below this sediment depth, egg densities decline. The highest egg densities were found in sediments under the deepest water. Diapausing eggs of L. minutus survive in the sediments at least two years, as shown by the recovery of the population after a year in which no new diapausing eggs were produced, and probably for two or more decades. Long-term dormancy can have the effect of ensuring the continuation of a population through periods of poor recruitment, and can help create conditions for the coexistence of competing species. Other investigators have suggested that S. oregonensis and L. minutus are competitors in other lakes when they co-occur.     

The effects of feeding damage in ragweed Ambrosia artemisiifolia (Asteraceae) on populations of Zygogramma suturalis (Coleoptera,Chrysomelidae)

Summary Field sampling indicated that the number of eggs laid by a Zygogramma suturalis female within a sampling plot correlated inversely with the mean degree of ragweed damage. Feeding on extensively damaged ragweed in the laboratory caused a drop in oviposition intensity, and a considerable proportion of females completely stopped oviposition. Feeding on slightly damaged ragweed had no significant effect on oviposition intensity. Ovipositing females preferred to feed on the intact ragweed and lay their eggs close to it. The locomotory activity of ovipositing females was significantly higher on highly damaged ragweed whereas non-ovipositing (diapausing) females and males were behaviourally indifferent to the extent of ragweed damage. Under natural conditions, ovipositing females more frequently left damaged host plants for less damaged one. If the degree of ragweed damage is high over a large area, the insects that were unable to find undamaged plants for several days oviposited less and some females entered diapause. The adaptive effect of these reactions is a decrease of population density in advance, before it might drop as a result of starvation. These results are in agreement with the second model of insect reaction to the damage-induced changes in a host plant (Edwards and Wratten 1987).     

Effects of thermophotoperiod on growth parameters of Helicoverpa armigera

The effects of photoperiod and temperature on growth parameters of Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) were investigated under laboratory conditions by exposing its larvae to fluctuating and alternating temperature regimes. Our data made evident that the interplay between photoperiod and temperature has a direct effect on growth parameter responses of H. armigera. However, the type of temperature regime (fluctuating or alternating) may enhance or diminish the effects of photoperiod. With fluctuating temperature, larval developmental time was significantly reduced with increasing photophase, irrespective of the diapause status later in the pupal stage; the lowest value was observed under continuous light conditions. With alternating temperature, larval developmental time was significantly decreased with the reduction in temperature amplitude, and with the coincidence of the thermophase with the scotophase. At both temperature regimes, no significant differences in pupal weight were observed between diapausing and non‐diapausing individuals, although, in most treatments, the diapausing pupae tended to be heavier than the non‐diapausing ones. The increased pupal weight of individuals destined for diapause is probably related to their longer larval developmental time. Knowing the effects of these factors on the variation of H. armigera growth is necessary in explaining phenomena associated with immature stages, and can lead to a more profound understanding of the potential for this insect to evolve in response to environmental changes.     

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

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Very long diapause and extreme resistance to population disturbance in a galling insect

1. Some insects have a prolonged diapause – a dormancy that extends over more than 1 year. In most species prolonged diapause involves one or a few extra years, but in extreme cases diapause may surpass 10 years. Few cases of very long diapause have been described, and very little is known about the population consequences of the temporal refuge formed by the diapausing individuals. 2. The gall midge Contarinia vincetoxici Kieffer galls the flowers of a long‐lived herb Vincetoxicum hirundinaria Med. After completing development, larvae leave the galls for the ground where they enter diapause. Extending an earlier published inoculation experiment, we show that the diapause may last up to at least 13 years, with a median duration of at least 6 years. 3. The gall midge is attacked by two parasitoid species. Dissections of gall midge larvae for presence of parasitoids revealed that Omphale salicis Haliday had a maximum 2 year diapause and Synopeas acuminatus Kieffer a maximum 4 years. The very long diapause of the gall midge may thus provide a temporal refuge from these enemies. 4. In a 15‐year field experiment all galls were removed every year from six isolated habitat patches. Density changes in experimental populations were not statistically different from control populations for over a decade. After 14–15 years a modest decline could be observed. This slow response illustrates that prolonged diapause in C. vincetoxici provides a very strong population buffer against mortality during the galling stage.     

The Insect Growth Regulator Pyriproxyfen Terminates Egg Diapause in the Asian Tiger Mosquito,Aedes albopictus

The Asian tiger mosquito, Aedes albopictus, is a highly invasive mosquito species that transmits chikungunya and dengue. This species overwinters as diapausing eggs in temperate climates. Early diapause termination may be a beneficial strategy for winter mosquito control; however, a mechanism to terminate the diapause process using chemicals is not known. We tested the hypothesis that a hormonal imbalance caused by the administration of juvenile hormone analog would terminate egg diapause in A. albopictus. We tested the insect growth regulator pyriproxyfen on all developmental stages to identify a susceptible stage for diapause termination. We found that pyriproxyfen treatment of mosquito eggs terminated embryonic diapause. The highest rates of diapause termination were recorded in newly deposited (78.9%) and fully embryonated (74.7%) eggs at 0.1 and 1 ppm, respectively. Hatching was completed earlier in newly deposited eggs (25–30 days) compared to fully embryonated eggs (71–80 days). The combined mortality from premature diapause termination and ovicidal activity was 98.2% in newly deposited and >98.9% in fully embryonated eggs at 1 ppm. The control diapause eggs did not hatch under diapausing conditions. Pyriproxyfen exposure to larvae, pupae and adults did not prevent the females from ovipositing diapausing eggs. There was no effect of pyriproxyfen on diapausing egg embryonic developmental time. We also observed mortality in diapausing eggs laid by females exposed to pyriproxyfen immediately after blood feeding. There was no mortality in eggs laid by females that survived larval and pupal exposures. In conclusion, diapausing eggs were the more susceptible to pyriproxyfen diapause termination compared to other life stages. This is the first report of diapause termination in A. albopictus with a juvenile hormone analog. We believe our findings will be useful in developing a new control strategy against overwintering mosquito populations.