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.     

Diapause in Monogonont Rotifers

This review focuses on more recent findings on the diapause in Monogonont rotifers, since the major reviews by Pourriot & Snell (1983, Hydrobiologia 104: 213–224) and Gilbert (1992, Rotifera. In Adiyodi, K. G. & R. G. Adiyodi (eds), Reproductive Biology of Invertebrates, Vol. 5 – Sexual Differentiation and Behaviour. IBH Publishing Co., Oxford: 115–136; Vol. 6A – Asexual Propagation and Reproductive Strategies. IBH Publishing Co., Oxford: 231–263.). It covers diapausing egg formation, diapausing egg survival, and diapausing egg hatching as well as possible strategies involved in these processes. Data from laboratory and field studies exist, but little information is available on diapausing egg hatching in the field. Resting or diapausing egg production can be mictic and in some cases amictic. Mictic diapausing egg production depends on the balance between cues promoting and inhibiting mictic female production. Such cues can be either environmental or endogenous. Our knowledge on factors inducing mixis is still limited to a few species, but effects of crowding on mixis induction may be more widespread. Recent results also show that male mating behavior may play an important role in the successful production of diapausing eggs. Hatching may be induced by factors related to temperature and light conditions; also desiccation may have a role. However, desiccation of temporary habitats may also be damaging to diapausing stages. Although few data are available, those existing point to distinct differences between populations and the importance of clonal variation within populations regarding the initiation as well as the termination of diapause.     

Adaptive latitudinal cline of photoperiodic diapause induction in the parasitoid Nasonia vitripennis in Europe

Living in seasonally changing environments requires adaptation to seasonal cycles. Many insects use the change in day length as a reliable cue for upcoming winter and respond to shortened photoperiod through diapause. In this study, we report the clinal variation in photoperiodic diapause induction in populations of the parasitoid wasp Nasonia vitripennis collected along a latitudinal gradient in Europe. In this species, diapause occurs in the larval stage and is maternally induced. Adult Nasonia females were exposed to different photoperiodic cycles and lifetime production of diapausing offspring was scored. Females switched to the production of diapausing offspring after exposure to a threshold number of photoperiodic cycles. A latitudinal cline was found in the proportion of diapausing offspring, the switch point for diapause induction measured as the maternal age at which the female starts to produce diapausing larvae, and the critical photoperiod for diapause induction. Populations at northern latitudes show an earlier switch point, higher proportions of diapausing individuals and longer critical photoperiods. Since the photoperiodic response was measured under the same laboratory conditions, the observed differences between populations most likely reflect genetic differences in sensitivity to photoperiodic cues, resulting from local adaptation to environmental cycles. The observed variability in diapause response combined with the availability of genomic tools for N. vitripennis represent a good opportunity to further investigate the genetic basis of this adaptive trait.     

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.     

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.     

Sexual reproduction and diapause of Hexarthra sp. (Rotifera) in short-lived ponds in the Chihuahuan Desert

1. In the life cycle of monogonont rotifers it is generally assumed that diapausing eggs invariably hatch into amictic stem females which produce female offspring parthenogenetically. Diapausing eggs are only produced by later generations after sexual reproduction has been induced by environmental cues. 2. We show that populations of an undescribed Hexarthra species inhabiting small temporary ponds in the Chihuahuan Desert deviate from this life cycle pattern. These ponds may dry within days and up to 85% of females were mictic. Females producing male offspring and diapausing eggs were observed 1 or 2 days, respectively, after ponds had filled with water. 3. Under laboratory conditions, 7–46% of females hatching from re‐hydrated sediments were sexual. Male offspring of these females can fertilise other mictic stem females leading to diapausing egg formation. In laboratory experiments, females produced fully developed diapausing eggs within 1.9 days at 20 °C and 1.2 days at 30 °C. 4. In addition, embryonic development time (1.1–0.3 days at temperatures between 12 and 30 °C) and juvenile period (2.1–0.5 days for the same temperature range) are shorter than those of other rotifer species. In short‐lived habitats, the potential for rapid population development and production of new diapausing eggs may be crucial in the long‐term survival of populations.     

Geographic variation in diapause induction: the grape berry moth (Lepidoptera: Tortricidae)

Diapause in insects occurs in response to environmental cues, such as changes in photoperiod, and it is a major adaptation by which insects synchronize their activity with biotic resources and environmental constraints. For multivoltine agricultural insect pests, diapause initiation is an important consideration in management decisions, particularly toward the end of the growing season. The grape berry moth, Paralobesia viteana (Clemens), is the main insect pest affecting viticulture, and this insect responds to postsummer solstice photoperiods to initiate diapause. Because the range of grape berry moth extends from southern Canada to the southern United States, different populations are exposed to different photoperiodic regimes. We quantified the diapause response in grape berry moth populations from Arkansas, Michigan, New York, Pennsylvania, Texas, and Virginia, and observed latitudinal variation in diapause initiation. Populations from Michigan, New York, and Pennsylvania responded significantly different than those from Arkansas, Texas, and Virginia. We also observed, as a consequence of our experiments, that the timing of our laboratory studies influenced grape berry moth's response to photoperiod, ceteris paribus. Experiments that were conducted when grape berry moth would be naturally in diapause resulted in a significant higher proportion of diapausing pupae at photoperiods (i.e., >15 h) that generally do not induce diapause, suggesting that attention should be paid to the timing of behavioral and physiological experiments on insects. This relationship between photoperiod and diapause induction in grape berry moth across geographic regions will provide applicable knowledge to improve pest management decisions.     

Genetic and phenotypic sources of life history variation along a cline in voltinism in the cricket Allonemobius socius

Clinal variation in life histories can be genetically based, resulting from selection imposed by different environments, or it may be due to the differential expression of phenotypically plastic traits. We examined the cline in voltinism in the egg-diapausing cricket Allonemobius socius, with populations spanning the switch from a univoltine to a bivoltine phenology. A common garden experiment was employed, using environments that mimicked photoperiod and temperature conditions found in the field. There were only small differences in development time among populations, and the difference in phenology observed in the field is likely due to clinal variation in the length of the growing season. We found large genetically-based differences in the reaction norm for egg diapause that were further magnified by environmental cues. The synergism of genetic and environmental effects was an example of cogradient selection. In the zone of transition between phenologies, voltinism appeared to be a conditional strategy, rather than a genetic polymorphism. First-generation females from this area can lay either direct-developing or diapause eggs depending on the likelihood that a second generation will have sufficient time to develop. For this species, the cline in voltinism is the result of a combination of environmental effects on development, and genetic and environmental influences on egg diapause propensity.     

Hatching phenology,life history and egg bank size of fairy shrimp Branchipodopsis spp. (Branchiopoda,Crustacea) in relation to the ephemerality of their rock pool habitat

In temporary aquatic habitats, permanence and the severe disturbance associated with desiccation are strong selective agents expected to lead to differentiation in life history strategies in populations experiencing different disturbance regimes. Besides optimal timing of hatching of dormant life stages, maturation and reproduction, pool inhabitants also benefit from the acquisition of reliable cues for the quality of the ambient environment. We investigated whether hatching patterns, life history characteristics and egg bank size of Branchipodopsis fairy shrimp (Branchiopoda, Anostraca) inhabiting a cluster of temporary rock pools in South Africa reflect variation in habitat stability and hatching cues. Long-term hydrological variation was used to select pools along a gradient of habitat stability. Initial conductivity was a good indicator for the length of inundations. No hatching occurred under elevated conductivities, which may present a mechanism to avoid abortive hatching. Egg bank size was unaffected by habitat size or habitat stability but instead was related to cover by a protective sheet of dry aquatic vegetation, which presumably counteracts egg bank erosion by wind when pools are dry. Life history but not hatching phenology reflected some aspects of habitat stability. Fairy shrimp populations in ephemeral pools started reproduction earlier than populations in more stable habitats. Additional common garden or transplant experiments, however, will be required to assess the relative importance of environmental and genetic components in explaining the observed variation and acquire more insight into the trade-offs that lie at the base of the evolution of life history strategies along the pond permanence gradient.     

Rapid seasonal adaptation of an alien bruchid after introduction: geographic variation in life cycle synchronization and critical photoperiod for diapause induction

Whether alien insects that are introduced into temperate regions adapt to seasonally changing environmental conditions is an important question in evolutionary biology. If rapid evolution has occurred in a non‐native environment, a latitudinal cline in critical photoperiod for diapause induction (i.e., the photoperiod at which half of the individuals enter diapause) and in life cycle synchronization with host plant phenology should be evident among locations. The alien bruchid Acanthoscelides pallidipennis (Motschulsky) (Coleoptera: Bruchidae) is native to North America and introduced into Japan with the host plant Amorpha fruticosa L. (Fabaceae) in the late 1940s. To examine whether seasonal adaptation has occurred in A. pallidipennis, we conducted a laboratory experiment and phenological observations using three latitudinally different populations. We bred F1 eggs at 22 °C and five photoperiodic regimens – L:D = 10:14, 13:11, 14:10, 15:9, or 16:8 hours – and examined whether diapause was induced. The estimated critical photoperiod for diapause induction was longest in the most northern population and shortest in the most southern population. Life cycle was found to be synchronized with host phenology in each location. Also voltinism varied geographically, from univoltine in the northern population to bivoltine in the southern populations. These results showed that A. pallidipennis rapidly adapted to seasonal environmental conditions in Japan after its introduction.     

Some principles of selecting natural material for rearing and the endogenous processes in laboratory strains of the blowfly <Emphasis Type="Italic">Calliphora vicina</Emphasis> R.-D. (Diptera,Calliphoridae)

The ability to enter reproductive and larval diapauses should be taken into account when natural populations of the blowfly Calliphora vicina are selected for laboratory rearing. The reproductive diapause occurring at 20–25° in some females retards their maturation and decreases the reproductive activity of the laboratory strain. On the other hand, diapausing females conditioned by low temperature may be used for temporary conservation of the strain. However, keeping the diapausing larvae is the most reliable way of storage. The endogenous variation of the incidence of larval (from 0 to 100%) and reproductive (from 0 to 55%) diapauses was observed in successive generations of several laboratory strains developing under constant photoperiodic and temperature conditions. The significance of such endogenous processes for interpretation of experimental data is discussed. For over 20 years of laboratory breeding of C. vicina, cases of strain depression were observed, when the number of the egg rafts decreased and then oviposition ceased, abnormal puparia appeared, the flies hardly emerged, etc. Such depressed strains may be revived by changing the photoperiodic regime.     

Egg development and diapause: ecophysiological and genetic basis of phenological polymorphism and adaptation to varied hosts in the green oak tortrix,Tortrix viridana L. (Lepidoptera: Tortricidae)

Experiments concerned 8 tortrix populations associated with varied oak species. They showed that the egg development included a phase of diapause. Completion of embryogenesis at 20 degrees C was used as a criterion for whether diapause was completed. Under semi-natural conditions diapause terminated in late autumn or early winter, then eggs developed continuously, without postdiapause winter quiescence, even in severe cold. The eggs from the populations associated with holm or cork oak completed diapause then hatched later than those from the populations associated with sessile or pubescent oak. Reciprocal crossbreedings confirmed that this phenological polymorphism was genetically determined. Under constant temperatures the physiological state of diapausing eggs, assessed by measuring their cold requirements to complete diapause by exposure to 8 degrees C, varied gradually with increasing age. This diapause development was strongly temperature-dependent. Cold requirements of diapausing eggs were much higher in a late-hatching than in an early-hatching population. This explains the phenological polymorphism of the tortrix: the more eggs need cold, the later they complete diapause in autumn, and the later they hatch in spring. Egg cold requirements varied widely within populations too, which resulted in large variations in the date of diapause end among individuals. The date of egg hatch was influenced by the temperatures occurring during diapause and postdiapause, but apparently not by photoperiod.     

Embryo ecology: Developmental synchrony and asynchrony in the embryonic development of wild annual fish populations

Embryo–environment interactions are of paramount importance during the development of all organisms, and impacts during this period can echo far into later stages of ontogeny. African annual fish of the genus Nothobranchius live in temporary pools and their eggs survive the dry season in the dry bottom substrate of the pools by entering a facultative developmental arrest termed diapause. Uniquely among animals, the embryos (encased in eggs) may enter diapause at three different developmental stages. Such a system allows for the potential to employ different regulation mechanisms for each diapause. We sampled multiple Nothobranchius embryo banks across the progressing season, species, and populations. We present important baseline field data and examine the role of environmental regulation in the embryonic development of this unique system. We describe the course of embryo development in the wild and find it to be very different from the typical development under laboratory conditions. Development across the embryo banks was synchronized within and across the sampled populations with all embryos entering diapause I during the rainy season and diapause II during the dry season. Asynchrony occurred at transient phases of the habitat, during the process of habitat desiccation, and at the end of the dry season. Our findings reveal the significance of environmental conditions in the serial character of the annual fish diapauses.     

Local adaptation of sex induction in a facultative sexual crustacean: insights from QTL mapping and natural populations of Daphnia magna

Dormancy is a common adaptation in invertebrates to survive harsh conditions. Triggered by environmental cues, populations produce resting eggs that allow them to survive temporally unsuitable conditions. Daphnia magna is a crustacean that reproduces by cyclical parthenogenesis, alternating between the production of asexual offspring and the sexual reproduction of diapausing eggs (ephippia). Prior to ephippia production, males (necessary to ensure ephippia fertilization) are produced parthenogenetically. Both the production of ephippia and the parthenogenetic production of males are induced by environmental factors. Here, we test the hypothesis that the induction of D. magna resting egg production shows a signature of local adaptation. We postulated that Daphnia from permanent ponds would produce fewer ephippia and males than Daphnia from intermittent ponds and that the frequency and season of habitat deterioration would correlate with the timing and amount of male and ephippia production. To test this, we quantified the production of males and ephippia in clonal D. magna populations in several different controlled environments. We found that the production of both ephippia and males varies strongly among populations in a way that suggests local adaptation. By performing quantitative trait locus mapping with parent clones from contrasting pond environments, we identified nonoverlapping genomic regions associated with male and ephippia production. As the traits are influenced by two different genomic regions, and both are necessary for successful resting egg production, we suggest that the genes for their induction co‐evolve.     

Seasonal adaptations of populations of the southwestern corn borer, Diatraea grandiosella, from tropical and temperate regions

Seasonal adaptations of populations of the southwestern corn borer, Diatraea grandiosella, obtained from south-central Mexico (19°N latitude) and southeast Missouri (37°N latitude) were compared. Day length and temperature were found to serve as environmental cues to programme the larval diapause of both populations, but different critical values were observed. The critical day length for diapause induction was about 13 hr light/day for Mexican larvae and about 15 hr light/day for Missouri larvae, and was relatively stable at 20 to 30°C. Mexican larvae displayed a less-intense diapause than did Missouri larvae. Some diapausing Mexican larvae maintained at 25 or 30°C pupated in about 15 days, regardless of the day length to which they were exposed. The rate of diapause development of Mexican larvae was high at day lengths between 14 hr and 16 hr, whereas that of Missouri larvae was accelerated at day lengths of 16 hr at 25 and 30°C. Diapause development of Mexican larvae was virtually unaffected by chilling at 10°C, whereas that of Missouri larvae continued at a low rate at 10°C. Selection of Mexican larvae for diapause showed that only four generations were needed to significantly increase the incidence of diapause.     

Embryonic diapause in the elasmobranchs

Embryonic diapause is a temporary suspension of development at any stage of embryogenesis, which prolongs the gestation period, allowing parturition to occur in conditions that are more suitable for newborns. This reproductive trait is widespread among all vertebrates, including elasmobranchs. Although it has only been confirmed in two elasmobranchs (Rhizoprionodon taylori and Dasyatis say), evidence indicates that at least 14 species of rays and two sharks undergo diapause, suggesting that this form of reproduction exists within a wide range of elasmobranch reproductive modes, including lecithotrophs and matrotrophs. Where it has been studied, embryogenesis is arrested at the blastodisc stage and preserved in the uterus for periods from four to 10?months. There are still many questions that remain unanswered concerning the knowledge on the biology of most diapausing species but it is clear that species benefit differently from this reproductive trait. As in other vertebrates, it is likely that environmental cues and hormones (especially progesterone and prolactin) are involved in the control of diapause in elasmobranchs, however rigorous testing of current hypothesis remains to be carried out.     

Dormancy, dispersal and the survival of cyclopoid copepods (Cyclopoida, Copepoda) in a lowland floodplain

1. The survival of cyclopoid copepods was investigated in a floodplain for 2 years where flooding occurred during the cold season. The cyclopoid community was studied in three waterbodies with distinct hydroperiods: a permanent pond connected to the flooded area during inundation, a temporary pool that is part of the flooded area and an isolated temporary pool.
2. Field studies, including data obtained from samples of water, sediment and soil, showed the overall predominance of species with a summer diapause over those with a winter diapause or without diapause. Emergence of cyclopoid copepods at the onset of flooding, examined using emergence traps and data from recently filled or still isolated temporary pools, showed that some species can survive several months of drying.
3. The ability of the diapausing fourth copepodid stages of Cyclops strenuus and C. insignis , the two cyclopoids most abundant during winter and spring flooding, to survive terrestrial conditions was tested in laboratory experiments. Both species survived for several months, but rates differed among the species. A higher percentage of C. strenuus survived for a longer period, possibly explaining why this species was relatively more abundant in more temporary habitats.
4. Both dormancy and dispersal facilitated survival of cyclopoid copepods in transient habitats connected to each other during flood periods. Dormancy was the most important survival strategy, whereas dispersal could be more important following prolonged periods without flooding.     

Overwintering survival and postdiapause fecundity in a population of the Kanzawa spider mite <Emphasis Type="Italic">Tetranychus kanzawai</Emphasis> (Acari: Tetranychidae) on <Emphasis Type="Italic">Orixa japonica</Emphasis> (Rutaceae)

In several adult-diapausing insects and mites, long duration of diapause decreases egg production after diapause termination. However, such nonlethal effects are much less studied than overwintering survival. In this study, lethal and nonlethal effects of different periods of diapause were investigated in an adult-diapausing spider mite, Tetranychus kanzawai Kishida (Acari: Tetranychidae), through field experiments. Diapausing females produced in the laboratory were kept in their natural habitat from October or November to the next April, and survival rate and postdiapause fecundity were compared between the months. The survival rate was lower, but not significantly, in the October treatment. Postdiapause fecundity was also not significantly different between the months. These results suggest that the effects of diapause on survival and reproduction are quite small after October, when diapausing mites are increasing in their natural habitat.     

Transgenerational phenotypic plasticity of diapause induction and related fitness cost in a commercial strain of the parasitoid Aphidius ervi Haliday

Diapause is an adaptation that insects have evolved to synchronize their life cycle with that of seasonal climatic changes and resources availability. However, cues for its induction are not always clear and, in some cases, a maternal effect may be involved. At the population level, just a part of the individuals may exhibit diapause with important consequences in terms of winter survival. Moreover, clear indicators of diapause state are difficult to identify. Diapause induction was thus investigated in the aphid parasitoid species Aphidius ervi Haliday (Hymenoptera: Braconidae) developing in the aphid Sitobion avenae (Hemiptera: Aphididae) at four crossed photothermal regimes (16 °C and 8 °C, 16:8 h L:D and 8:16 h L:D), and during 2 successive generations. We analyzed the reliability of changes in mummy color to assess for the diapausing state compared to dissections, and we measured parasitoid morphological and physiological traits. We observed that the proportion of dark brown mummies increased after one generation under low photothermal regime compared to other regimes. No diapause was recorded at 16 °C, 16:8 h L:D, while we observed 16.2% and 67.5% diapause incidence at 8 °C, 8:16 h L:D, at 1st and 2nd generation, respectively. Diapause induction is thus increased by short day-length conditions and low temperatures as well as by maternal effects. All parasitoid life-history traits (weight, size, fat content, water content, egg-load, and longevity) were affected by the photothermal regime and/or the generation. These results raise new questions on the environmental thresholds needed to induce diapause and on survival and adaptation potential of commercially available parasitoid strains in different environments.