Ground crickets singing in volcanic warm “islets” in snowy winter: Their seasonal life cycles,photoperiodic responses and origin

The ground cricket Dianemobius nigrofasciatus overwinters as an egg in Japan, being univoltine in Hokkaido and northern Honshu and bivoltine farther south. In Hokkaido, however, this cricket is heard singing in winter in several fumarolic fields covered with moss and grasses locally known as “bokke”. In such warm “islets” the adult density was high in early summer and again in autumn, indicating that the cricket is bivoltine in contrast to the univoltine life cycle outside the bokke habitats in Hokkaido. Eggs laid by females collected at regular intervals from a bokke habitat showed a clear seasonal cycle of diapause incidence. At 26°C, the bokke strains produced non‐diapause eggs under long days and diapause eggs under short days as in the southern bivoltine populations, although the critical day‐length was longer than in the south. Several strains derived from non‐bokke habitats in Hokkaido and northern Honshu produced high percentages of diapause eggs under long days as well as short days as expected for the univoltine life cycle. Winter adults singing in bokke habitats could be either survivors of the autumn generation or individuals derived from eggs laid in autumn and then matured in response to the high soil temperature. In the laboratory, the proportion of egg diapause in short days was decreased by selection only for several generations. Phylogenetic trees of bokke and non‐bokke populations, based on both the nucleotide sequence of the mitochondrial COI gene and four allozyme loci, suggest that bokke populations have not been isolated from non‐bokke populations for an evolutionarily significant time.     

Effect of variation in photoperiodic response on diapause induction and developmental time in the willow leaf beetle, Plagiodera versicolora

The willow leaf beetle, Plagiodera versicolora (Coleoptera: Chrysomelidae) overwinters in adult diapause. In this study, the photoperiodic responses for diapause induction and developmental time were examined in the Ishikari (Hokkaido, Japan) population of P. versicolora. All females entered reproductive diapause under short daylength (L10:D14), but 31.7% of females did not enter diapause under long daylength (L16:D8). The developmental time from oviposition to adult emergence was significantly longer at L10:D14 than that at L16:D8. Norm of reaction curves illustrated variation among families in the photoperiodic responses for diapause induction and for developmental time. ANOVA indicated significant family × photoperiod interactions in the developmental time. At L16:D8, developmental time was positively correlated with the incidence of diapause in females. This means that a female having a longer developmental time tends to have a longer critical photoperiod. Such variation may be maintained by differences in selection pressures on the growth rate and the critical photoperiod for diapause induction between univoltine and bivoltine genotypes because Ishikari is located in a transitional area between populations with univoltine and bivoltine life cycles.     

The role of gene flow asymmetry along an environmental gradient in constraining local adaptation and range expansion

Theoretically, asymmetric gene flow along an environmental gradient can limit species range expansion by keeping peripheral populations from locally adapting. However, few empirical studies have examined this potentially fundamental evolutionary mechanism. We address this possibility in the cricket Allonemobius socius, which exist along a season‐length gradient where the probability of producing a single generation per year (univoltinism) increases with latitude. As the probability of univoltinism increases northwards, populations are expected to hedge their bets by producing a greater proportion of diapause eggs when exposed to a mild diapause cue. However, gene flow from southern populations may disrupt local adaptation in the north by reducing the proportion of diapause eggs (expected to be 100% in pure univoltine environments). This may limit range expansion along the northern periphery where A. socius compete with A. fasciatus, a sister species that exhibits an invariant diapause‐only egg‐laying strategy. To assess the potential for range limitation, we examined diapause incidence (the proportion of diapause eggs produced under diapause conditions), gene flow symmetry and population structure across nine A. socius populations. We found that gene flow was asymmetric and biased northwards towards the periphery. Furthermore, peripheral populations that inhabited pure univoltine environments produced numerous nondiapause eggs (a southern, bivoltine diapause phenotype), which we assume to be a suboptimal phenotype. These patterns suggest that asymmetric gene flow along the gradient constrains adaptation in peripheral populations, potentially constraining species range expansion.     

Variability of photosensitive period and voltinism among populations of a butterfly,Ypthima multistriata,inhabiting similar latitudes and altitudes

In Ypthima multistriata Butler (Lepidoptera: Nymphalidae), there are univoltine and bivoltine populations in adjacent areas with similar climatic conditions. A previous study revealed that larvae of both univoltine and bivoltine populations diapause under a constant short day (i.e., a constant short light period; L13:D11), but not under a constant long‐day condition (L16:D8). However, in both types of populations, adults of an overwintering generation appear and oviposit in June and soon thereafter larvae hatch. Therefore, the younger larvae (at least the first instars) of both types of populations experience a long day; nevertheless, the larvae of univoltine populations diapause in nature. To resolve this inconsistency, we set up two hypotheses: (1) the photosensitive stage of larvae is the second instar or later, and (2) the photosensitive stage of univoltine populations is later than that of bivoltine populations. To test these hypotheses, we performed rearing experiments with two univoltine populations and two bivoltine ones. The results indicated that the photosensitive stage was the second or third instar and that the photosensitive stage was later in one univoltine population than in the two bivoltine populations. Larvae of the other univoltine population diapaused under all conditions. The former result supports our hypothesis, and the latter result indicates that the response to photoperiod is different among univoltine populations. In addition, larval development was slower in one univoltine population than in the bivoltine populations, which also delays the timing of the diapause decision in this univoltine population. Larvae that experienced a long day during the first and middle instars but experienced a short day at the end of their larval stage developed faster than larvae that experienced a constant long day. This may be an adaptation to enable emergence before the start of a cold season that is unsuitable for reproduction.     

Female mating frequency in a wild population of scorpionflies (Panorpa germanica, Panorpidae, Mecoptera)

In this study, we investigated mating frequencies of female scorpionflies Panorpa germanica in the field using two different experimental approaches. First, the mating status of wild‐caught females was estimated on the basis of sperm numbers present inside their sperm storage organs. Secondly, the number of mating partners wild‐caught females must have had was inferred from mother‐offspring analyses of a polymorphic microsatellite locus. Our results suggest a very low mating frequency of wild female P. germanica. Consequently, the risk of sperm competition is rather low in this species. The relevance of female mate choice in relation to the low mating frequency is discussed.     

Life‐history traits related to diapause in univoltine and bivoltine populations of Ypthima multistriata (Lepidoptera: Satyridae) inhabiting similar latitudes

In most temperate insects, diapause strategies and voltinism generally exhibit latitudinal clines, supporting the concept that they represent adaptations to climate. In contrast, in the satyrine butterfly Ypthima multistriata Butler, local populations with different voltinism patterns are geographically intermingled, suggesting that life‐history traits related to diapause may differ even between geographically and phylogenetically close populations. In this study, we experimentally examined the critical photoperiod for diapause induction and the larval developmental period in two univoltine and two bivoltine populations of Y. multistriata, all of which inhabit virtually the same latitude (34.652–34.750°N). We found that the critical photoperiod for diapause induction was longer in the univoltine populations than in the bivoltine populations. Moreover, the larval period under the long day length treatment was different among populations in both sexes, although significant differences were also detected between populations with the same voltinism. These results indicate that in Y. multistriata, life‐history traits related to diapause can not be attributed merely to climatic conditions such as temperature or day length, which depend largely on latitude. Therefore, we suggest that biotic elements, such as leaf toughness, as well as abiotic elements should be taken into account in attempts to explain the enigmatic pattern of geographic variation in the diapause strategies of Y. multistriata.     

Nutrition‐ and sex‐dependent utilization of body resources in relation to reproduction in a scorpionfly

Reproduction often comes at a cost of a reduction in body functions. In order to enhance their reproductive output, some insect species degenerate their thoracic muscles, typically resulting in reduced flight ability. From a life‐history trade‐off perspective, we expect the importance of body resource utilization to be amplified both with increased reproductive expenditure and with increased resource limitation. In this study, we measured age‐related changes in thorax weight, as a measure of flight muscle size, during a major part of the adult lifespan in males and females of the scorpionfly Panorpa vulgaris. The aim of the study was twofold: first to investigate whether scorpionflies have the potential to degenerate their flight muscles; second, and more importantly, to determine whether the magnitude of flight muscle degeneration is a plastic response in relation to resource availability, and if it differs between the sexes. The results clearly demonstrate that food availability does influence investment in flight muscle development. The build‐up of the thoracic muscles was strongly influenced by nutrient availability. Furthermore, the age‐related decrease in thorax weight was significantly different for males and females. Only females showed a strong age‐dependent decrease in thorax weight, indicative of muscle degeneration, yet no difference between food treatments was detected. For males, there was no significant directional change in thorax weight. Nevertheless, with increasing age, the difference in thorax weight between food treatments increased significantly. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 102 , 199–207.     

Latitudinal clines in alternative life histories in a geometrid moth

The relative roles of genetic differentiation and developmental plasticity in generating latitudinal gradients in life histories remain insufficiently understood. In particular, this applies to determination of voltinism (annual number of generations) in short‐lived ectotherms, and the associated trait values. We studied different components of variation in development of Chiasmia clathrata (Lepidoptera: Geometridae) larvae that originated from populations expressing univoltine, partially bivoltine or bivoltine phenology along a latitudinal gradient of season length. Indicative of population‐level genetic differentiation, larval period became longer while growth rate decreased with increasing season length within a particular phenology, but saw‐tooth clines emerged across the phenologies. Indicative of phenotypic plasticity, individuals that developed directly into reproductive adults had shorter development times and higher growth rates than those entering diapause. The most marked differences between the alternative developmental pathways were found in the bivoltine region suggesting that the adaptive correlates of the direct development evolve if exposed to selection. Pupal mass followed a complex cline without clear reference to the shift in voltinism or developmental pathway probably due to varying interplay between the responses in development time and growth rate. The results highlight the multidimensionality of evolutionary trajectories of life‐history traits, which either facilitate or constrain the evolution of integrated traits in alternative phenotypes.     

Heterodynamic processes in Coccinella septempunctata L. (Coccinellidae: Coleoptera): a mini review

Among ladybirds, diapause has evidently been most studied in Coccinella septempunctata L. adults. Coccinella septempunctata (C‐7), the seven spot, has attracted attention both in Europe and the USA for being heterogeneous as to the induction of diapause. A polyphenic character of diapause is a prominent feature in C. septempunctata and this phenomenon generally and often generates voltinism heterogeneity within populations. A greater part of the C‐7 population shows an obligatory univoltine cycle, whereas a smaller proportion is facultatively polyvoltine. Coccinella s. bruckii in Japan is bivoltine, in which the first generation of adults aestivate while the second generation hibernates. This paper reviews this heterodynamic cycle and its importance in the life history of C‐7, as reported from different regions of the world. Heterogeneous voltinism and diapause smooth the progress of a portion of C‐7 populations to take benefit of aphids well into late summer and autumn. Understanding such variation and plasticity in the life history of this species can help in organizing proper biological control attempts using it as a biocontrol agent.     

Diapause and overwintering of two spruce bark beetle species

Diapause, a strategy to endure unfavourable conditions (e.g. cold winters) is commonly found in ectothermic organisms and is characterized by an arrest of development and reproduction, a reduction of metabolic rate, and an increased resistance to adversity. Diapause, in addition to adaptations for surviving low winter temperatures, significantly influences phenology, voltinism and ultimately population growth. We review the literature on diapause and overwintering behaviour of two bark beetle species that affect spruce‐dominated forests in the northern hemisphere, and describe and compare how these strategies can influence population dynamics. The European spruce bark beetle Ips typographus (L.) (Coleoptera, Curculionidae) is the most important forest pest of Norway spruce in Europe. It enters an adult reproductive diapause that might be either facultative or obligate. Obligate diapausing beetles are considered strictly univoltine, entering this dormancy type regardless of environmental cues. Facultative diapausing individuals enter diapause induced by photoperiod, modified by temperature, thus being potentially multivoltine. The spruce beetle Dendroctonus rufipennis (Kirby) (Coleoptera: Curculionidae) infests all spruce species in its natural range in North America. A facultative prepupal diapause is averted by relatively warm temperatures, resulting in a univoltine life cycle, whereas cool temperatures induce prepupal diapause leading to a semivoltine cycle. An adult obligate diapause in D. rufipennis could limit bi‐ or multivoltinism. We discuss and compare the influence of diapause and overwinter survival on voltinism and population dynamics of these two species in a changing climate and provide an outlook on future research.     

Diapause decision in the small tortoiseshell butterfly,Aglais urticae

Insects in temperate areas spend the inhospitable winter conditions in a resting stage known as diapause. In species that diapause in the larval or pupal stage, the decision whether to diapause or develop directly is customarily taken during the late instars, with long days (i.e., long light phases) and high temperatures promoting direct development. Among butterflies that overwinter as adults, data are rare and variable, but imply that the larval daylength conditions can affect the pathway decision. We studied the small tortoiseshell, Aglais urticae L. (Lepidoptera: Nymphalidae, Nymphalini), which is partially bivoltine from Central Scandinavia and southwards, and tested whether the pathway decision is taken in the larval or adult stage. We reared larvae under long‐day (L22:D2) or short‐day (L12:D12) photoperiods, and recorded the pathway taken by the eclosing adults by scoring their propensity to mate and produce eggs. We also tested whether the larval photoperiod influenced adult ability to diapause by assessing adult survival. The results clearly indicate that (1) there is no detectable effect of larval photoperiod treatment on the pathway decision taken by adults whether to enter diapause or to develop directly, (2) some individuals are obligately univoltine and insensitive to photoperiod during adulthood, whereas (3) other individuals can facultatively enter diapause or direct development, depending on the photoperiod experienced after adult eclosion.     

Diapause induction and termination in a commonly univoltine leaf beetle (Phratora vulgatissima)

Abstract The leaf beetle Phratora vulgatissima (Linnaeus 1758) is commonly univoltine in south‐central Sweden but may sometimes initiate a partial second generation. The current study was set out to investigate under what abiotic conditions the beetles initiate a second generation. Using climate chamber experiments, the beetles were shown to have a facultative reproductive diapause induced by declining day‐length. The critical day‐length (CDL) for diapause induction was estimated to be 18 h and 10 min. In the field, first‐generation beetles developing to adulthood before August in 2009 became reproductively active and produced a second generation, but most individuals emerged later and were in reproductive diapause. P. vulgatissima overwinter as adults and diapause was shown to be maintained until mid‐winter in 2008/2009. The cumulative temperature requirement for oviposition after diapause termination was estimated to be 222 day‐degrees with a 5.5°C temperature threshold. Three different day‐degree models that were developed to predict the phenology of female oviposition in the spring were validated by comparing model results with field data on the timing of oviposition in previous years. The study suggests that P. vulgatissima may initiate a second generation in Sweden if development of the first generation is completed before August. Warmer spring and summer temperatures due to ongoing climate change may cause advanced insect phenology and faster completion of insect life‐cycles at northern latitudes, which will affect the proportion of insects that initiate a second generation.     

Diapause and diapause dynamics of Colias alexandra (Lepidoptera: Pieridae)

Summary The mechanisms and adaptations involved in the obligate third instar larval diapause of Colias alexandra, a native Rocky Mountain and intermountain region butterfly, are examined. Generally univoltine throughout its distribution, scattered, isolated bivoltine populations occur. Factors influencing continuous development were investigated under laboratory conditions on a single generation of offspring from a univoltine population each year from 1976–1979. If exposed to mean temperatures >24°C during the second instar, a significant number of larvae fail to diapause. These results are interpreted in the context of the actual environmental conditions experienced by the univoltine source population and a bivoltine population. A high degree of individual variability in response to continuous development conditions is shown. Variation in certainty of diapause, within an originally univoltine population, could be the evolutionary starting point for evolving a genuine multivoltine cueing system and provide the mechanism for ecological range expansion.     

Fitness consequences of alternative life histories in water striders,Aquarius remigis (Heteroptera: Gerridae)

Using field and laboratory observations and experiments over 3 years, I investigated whether reproductive trade-offs shape individual life histories in two natural populations of the water strider, Aquarius remigis, in which univoltine and bivoltine life cycles coexist. Both later eclosion dates and food shortages, even after adult eclosion, induced diapause in females, thus deferring reproduction to the following spring. Adult body size was positively affected by food availability during juvenile development. Higher food levels also increased the reproductive output of females, but not their longevity or oviposition period. When compared to spring breeders (univoltine life cycle), direct (summer) breeders (bivoltine life cycle) experienced reduced lifetime egg numbers and longevity, as well as reduced survivorship of their second-summer-generation offspring; these reproductive costs offset, at least in part, the advantage in non-decreasing populations of having two generations per year. Fecundity was correlated with body size, and among summer-generation females direct breeders were larger than non-breeders. The time remaining before the onset of winter and/or the time since adult eclosion augmented cumulative energy uptake, and consequently the lipid reserves and winter survival probability of non-breeding (diapausing) summer adults approaching hibernation. Overwintered spring reproductives died at faster rates than non-reproductive summer individuals despite greater food availability in spring, indicating a mortality cost of reproduction. Body length correlated with absolute and not with proportional lipid content but showed no consistent relationship with survivorship in the field. These results are in agreement with current theory on the evolution of insect voltinism patterns, and further indicate high degrees of life history flexibility (phenotypic plasticity) in the study populations in response to variable environmental factors (notably photoperiod and food availability). This may be related to their location in a geographic transition zone from uni- to bivoltine life cycles.     

Effect of photoperiod on winter and summer diapause of the soybean pod borer Leguminivora glycinivorella (Lepidoptera: Tortricidae)

To understand the geographical differences between diapause systems and synchronization of adult occurrence in the soybean pod borer Leguminivora glycinivorella (Lepidoptera: Tortricidae), we examined the timing of winter diapause termination and intensity of summer diapause using univoltine and potentially bivoltine individuals in Iwate, Japan. In laboratory rearing experiments of mature larvae maintained at constant temperature (20 °C), winter diapause intensity weakened by January without photoperiodic responses. Meanwhile, summer diapause was maintained by the long day length and presumably terminated with the photoperiodic transition from long to short day length. The intensity of summer diapause was stronger for cocoons that transitioned from a 16 h light to 8 h dark (LD 16:8) to a LD 15:9 photoperiod than for those that transitioned from LD 15:9 to LD 14:10. These results suggest that populations distributed in relatively low-latitude areas, with partly or potentially bivoltine individuals, would have a weaker summer diapause or none at all. Moreover, sexual differences in the number of days to emergence were not detected when individuals experienced a photoperiodic transition from long to short day length, suggesting that the summer diapause system may function to synchronize the emergence of males and females in the population examined.     

A secondary sex trait under construction: age- and nutrition-related salivary gland development in a scorpionfly (Insecta: Mecoptera)

Males of Panorpa vulgaris Imhoff and Labram, 1836 (Insecta: Mecoptera) can apply three alternative mating tactics to gain access to female mating partners: (1) without nuptial feeding, (2) providing females with a dead arthropod or (3) producing salivary masses. Providing females with salivary masses during copulation leads to the highest reproductive success, as it results in longer mating durations relative to the other tactics. While the number of sperm transferred correlates with the duration of copulation, the sperm of different males are used according to the fair raffle model. Therefore, salivary mass production is an important fitness determining factor for males. In order to provide females with salivary masses, males must first produce and store saliva secretion inside their salivary glands. The present study was concerned with the development of male salivary glands (= production of saliva) in the course of time after adult emergence. We can show that saliva production did not start before adult emergence, that the state of development of salivary glands was affected by larval nutrition as well as by adult nutrition and, moreover, by age. Older individuals had developed glands of greater mass than had younger animals. After receiving a one‐time feeding immediately after eclosion salivary gland mass increased, while body mass decreased with age. Therefore, male P. vulgaris were able to enlarge the amount of their mating resources (= saliva) independently from external nutritional supply (after the initial feeding) and at the expense of losing weight. Possible reasons and functional explanations are discussed.     

Life histories and mating system aspects of two Caucasian scorpionfly species: Panorpa similis Esben-Petersen and Panorpa connexa Mac Lachlan

Panorpa similis Esben-Petersen and Panorpa connexa MacLachlan are the most prominent Mecoptera in the Caucasian region. As our knowledge of mating systems and life histories of the different Panorpa species is unsatisfactory, it is the purpose of this contribution to add some interesting information on the life histories and mating behaviour of these two species. Further, we present results on successful breeding of these species, both in the field and the laboratory. Our data suggest that both species are monovoltine under the natural conditions in the Caucasian region, although our breeding experiments revealed a cryptic photoperiodic responsibility in a certain percentage of individuals of Panorpa connexa, which is completely absent in Panorpa similis. First, results on temporally and spatially differing foraging manners of the two species are presented. Male mating tactics of both species comprise copulations with one salivary mass as nuptial gift or copulations without any nuptial gift, but always without the use of force. This paper also gives information on egg deposition, egg hatching and larval development. Finally, we compare aspects of the mating systems for both species with those that have already been investigated for other Panorpa species.     

ADAPTATION TO SEASONALITY IN A CRICKET: PATTERNS OF PHENOTYPIC AND GENOTYPIC VARIATION IN BODY SIZE AND DIAPAUSE EXPRESSION ALONG A CLINE IN SEASON LENGTH

This paper investigates patterns of phenotypic variation in the striped ground cricket (Allonemobious fasciatus) along a cline in season length and tests the hypothesis that variation in body size and diapause propensity is the result of diversifying selection due to different local conditions. We examined 83 populations and found that A. fasciatus produced a single generation per year (univoltine) north of 37°N latitude and was bivoltine south of 35°30′N. Body size generally increased with increasing season length, with a sudden drop in the region corresponding to the transition from univoltine to bivoltine life cycles, reflecting the division of total season length in two within-bivoltine populations. We reared ten populations in our laboratory and found that much of the interpopulation variance in body size observed in the field could be attributed to genetic differences. Diapause expression also varied significantly among populations and was strongly correlated with season length. The heritability of body size did not differ between populations, but full-sib estimates greatly exceeded parent–offspring estimates suggesting that there are important nonadditive genetic effects. The heritability of diapause expression, determined from analysis of full sibs, varied significantly between populations (0.33 ± 0.10 to 1.31 ± 0.21) with an average of 0.74 ± 0.16. Body size and diapause expression were genetically correlated in transition-zone populations, but not in univoltine or bivoltine populations. Our findings support the suggestion that clinal variation in body size and diapause expression in the striped ground cricket reflect adaptation to season length.     

Genome‐wide microarray screening for Bombyx mori genes related to transmitting the determination outcome of whether to produce diapause or nondiapause eggs

The bivoltine silkworm Bombyx mori (Lepidoptera: Bombycidae) exhibits a maternally controlled embryonic diapause. Maternal silkworms decide whether to lay diapause or nondiapause eggs depending on environmental factors such as the temperature and photoperiod during the egg and larval stages, and then induce diapause eggs during the pupal stage. However, little is known about the molecular mechanism that conveys the outcome of whether to produce diapause or nondiapause eggs from the egg or larval stages to the pupal stage. This study used microarray analysis to investigate differentially expressed genes in the larval brains of diapause‐ and nondiapause‐egg producers, to which bivoltine silkworms were destined by thermal or photic stimulation during the egg stage. The cytochrome P450 18a1 and Krüppel homolog 1 genes were upregulated in producers of diapause eggs compared with those of nondiapause eggs under both experimental conditions. Cytochrome P450 18a1 encodes a key enzyme for steroid hormone inactivation and Krüppel homolog 1 is an early juvenile hormone‐inducible gene that mediates the repression of metamorphosis. The upregulation of these genes during the larval stage might be involved in the signaling pathway that transmits information about the diapause program from the egg stage to the pupal stage in the silkworm.     

Morphological Variation of the Scorpionfly Panorpa obtusa Cheng (Mecoptera: Panorpidae) with a New Synonym

Background

The overabundance of synonyms is an unavoidable by-product of taxonomic practice in insects. How to reduce or even eliminate synonymy has long been a great challenge for insect taxonomists. The scorpionflies Panorpa obtusa Cheng, 1949 and Panorpa leei Cheng, 1949 (Insecta: Mecoptera: Panorpidae) were originally described from Taibaishan in the Qinling Mountains with identical collection data and both are based on a single gender, the former on a male and the latter on two females. However, whether P. leei is conspecific with P. obtusa or a good species remains an unsolved problem.

Results

On the basis of intensive morphological comparison of 93 males and 53 females of scorpionflies collected from the type locality using light and scanning electron microscopy, we found P. obtusa has considerable morphological variation (especially the wing markings and genitalia in both male and female), and Panorpa leei is totally comprised of one of the morphs of P. obtusa.

Conclusions

In combination with identical type localities and overlapping morphological variation, P. leei Cheng is proposed as a junior subjective synonym of P. obtusa Cheng. To avoid synonyms, taxonomists should pay more attention to individual variation and base decisions on a series of specimens to describe new species.