Distribution of crustacean diapause: micro- and macroevolutionary pattern and process

Theoretical predictions for the relationships between duration of dormancy, reproductive life span, and dispersal ability developed for plants in temporally varying environments are applied here to crustaceans. Mathematical models suggest that diapause duration should negatively covary with adult life span, and that both diapause and life span should negatively covary with dispersal ability. A survey of 167 crustacean species from 20 orders and three classes confirms that species with prolonged diapause have short adult life spans and those with long adult lives either have diapause lasting less than a year, or do not diapause at all. Prolonged diapause is more common among small or inland water crustaceans than it is among large or marine species, whereas large or marine species have significantly longer adult life spans on average than do those that are small or from inland waters. A greater fraction of species in the Branchiopoda exhibit prolonged diapause than do members of the Maxillopoda which, in turn, are more likely to exhibit prolonged diapause than are the Malacostraca. A greater fraction of malacostracan species have adult life spans exceeding one year than do species in either the Branchiopoda or the Maxillopoda. Cladistic analysis shows that phylogenetic constraint is likely to be at least in part responsible for the expression of diapause among the Crustacea. We conclude that both natural selection and macroevolutionary pattern have influenced the distribution of diapause among modern crustaceans.     

Diapause, a potent force in the evolution of freshwater crustaceans

After a brief historical review of the discovery of diapause in freshwater crustaceans, its dramatic nature in certain cyclopoid copepods, in which diapausing individuals may occur at densities of > 10⁶ per m², is used to illustrate the enormous ecological significance of the phenomenon. Some of the problems presented by dispause in cyclopoid copepods are noted, including the different behaviour in different lakes of what appears to be a single species. Different physiological cues or different genetic endowments are clearly involved.The wider incidence of diapause in freshwater copepods and ostracods is noted.Among freshwater crustaceans it it the Branchiopoda that have universally adopted diapause, always at the egg stage. Even such an ancient order as the Anostraca, perhaps the most primitive of all crustaceans, produces elaborately constructed resting eggs that are capable of cryptobiosis, can remain viable in a dry state for long periods, and can tolerate extreme conditions. The nature of branchiopod resting eggs is briefly reviewed. Of these, only those of the Anomopoda are protected by containers derived from the parental carapace. These are mechanically complex in the most advanced species but, as shown by fossils, are extremely ancient structures.Factors initiating the onset and termination of diapause in branchiopods are briefly noted, and the process of hatching of resting eggs is outlined.     

Diapause in the seasonal cycle of stink bugs (Heteroptera,Pentatomidae) from the Temperate Zone

The paper reviews the data on diapause and related phenomena in stink bugs (Heteroptera: Pentatomidae). Using stink bugs as examples, the consecutive stages of the complex dynamic process of diapause (such as diapause preparation, induction, initiation, maintenance, termination, post-diapause quiescence, and resumption of direct development) are described and discussed. Out of 43 pentatomid species studied in relation to diapause in the Temperate Zone up to date, the majority (38 species) overwinter as adults, two species—as eggs, and another two species—as nymphs. Pentatoma rufipes is believed to be able to overwinter at different stages of its life cycle. Less than 5 % of pentatomid species are probably able to overwinter twice. Only five species have obligate diapause, others have the facultative one. Day-length and temperature are the main diapause inducing factors in the majority of species. The role of food in the control of seasonal development is essential in the pentatomid species feeding on plant seeds. In different species, different stages are sensitive to day-length. Some pentatomids retain sensitivity to photoperiod even after diapause, others lose it and become photo-refractory (temporarily or permanently). In Pentatomidae, such seasonal adaptations as photoperiodic control of nymphal growth rates, seasonal body colour change, migrations, and summer diapause (aestivation) are widely represented, whereas wing and/or wing muscle polymorphism has not been reported yet. In the subfamily Podopinae, induction of facultative reproductive winter diapause is under the control of photoperiod and temperature. All species feed on seeds and their seasonal development to a great extent reflects availability of food. However, the same food preferences and pattern of seasonal development are also characteristic to many species from the subfamily Pentatominae. All species of the subfamily Asopinae are predators. Among them, Picromerus bidens and Apateticus cynicus have obligate embryonic winter diapause, which is rear among true bugs. At the same time, A. cynicus and Podisus maculiventris belong to the same tribe but have different types of diapause: obligate embryonic diapause in A. cynicus and facultative adult diapause in P. maculiventris. Other Asopinae species studied up to date have facultative adult diapause controlled by photoperiod and temperature with probably only one exception: in Andrallus spinidens, adult diapause is controlled by temperature, and photoperiod plays only a secondary role. Thus, in spite of the similar habits and feeding types among Asopinae, the species of this subfamily have different types of diapause and the latter is controlled by different factors. In the subfamily Pentatominae, most species overwinter as adults and induction of their diapause is controlled by the long-day type photoperiodic response, in spite of the differences in their feeding preferences (within phytophagy). However, there are some exceptions in this subfamily, too: Palomena prasina, P. angulosa and Menida scotti have obligate diapause, which conditions univoltinism in these pentatomids. In M. scotti, only females have obligate adult diapause, whereas males remain physiologically active through the whole winter, this pattern being unusual for Heteroptera. The univoltine seasonal cycle of this species with summer diapause (aestivation) and apparent migrations is similar to that of shield bugs (Scutelleridae). According to the analysis of seasonal development, the evolution of seasonal adaptations in Pentatomidae does not directly reflect their phylogeny. However, individual genera, small tribes or even subfamilies have similar complexes of seasonal adaptations. At the same time, Pentatominae is a large and apparently collected taxon, but most of species in this subfamily have the same facultative adult diapause.     

桡足类滞育规律研究

首次提出用滞育指数对桡足类滞育能力进行相对量化处理 ,并对 10 2种桡足类的滞育能力同迁移能力、体长、栖息地之间的关系进行了数学分析 ,初步得出了滞育在桡足类中的分布规律 :在桡足类中滞育与迁移呈负相关 ,两者之间存在一定程度的置换 ;个体较小的桡足类一般具有较强的滞育能力和较弱的迁移能力 ,个体较大的桡足类一般具有较弱的滞育能力和较强的迁移能力 ;淡水桡足类一般比海洋桡足类具有较强的滞育能力。最后探讨了这种分布模式的成因     

Dormancy patterns in rotifers

Dormancy is common among rotifers: monogononts produce resting eggs (diapause) commonly after switching to mictic phase, and bdelloids enter anhydrobiosis (quiescence) at any time during their life cycle. Monogononts are short-lived and inhabit coarse-grained environments; their dormancy is a long-lasting diapause, commonly initiated by indirect remote cues. Bdelloids live 3 times as long, live in fine-grained environments and enter short-lasting quiescence as a direct response to changing environment. The two dormancy forms of the rotifers can be related to the temporal variation of their environments and seem to represent diverse responses to disturbance occurring at different rates. The two strategies are alternative and mutually exclusive, as no single rotifer species seems capable of both diapause and quiescence. Dormancy has great ecological significance: it can carry the population through stressful conditions, promote species coexistence and serve as a biodiversity bank providing reliable colonization source.     

Patterns of composition and species richness of crustaceans and aquatic insects along environmental gradients in Mediterranean water bodies

Differences in the dynamics of ecological processes between Mediterranean and colder temperate aquatic systems could imply different patterns in faunal communities in terms of composition and biodiversity (i.e. species richness and rarity). In order to identify some of these patterns the crustacean and aquatic insect composition and biodiversity of four water body types, classified according to their salinity and water permanence, were compared. Moreover, the relationships between species richness and water, pond and landscape variables were analysed. A total number of 91 water bodies located throughout Catalunya (NE Iberian Peninsula) were sampled. Three species assemblages were observed: one for permanent freshwaters, another for temporary freshwaters, and a third one for saline waters (SW), since permanent and temporary saline water bodies had similar composition. Differences in salinity were associated with proportion of crustaceans versus insects and with singularity. Thus, saline ponds had a higher proportion of crustaceans, and lower values of singularity. Conductivity was significantly related to total (crustaceans plus insects) richness, and also related to insect richness. The main difference between the models obtained for crustacean species richness and insect species richness is the significance of landscape variables in the latter, and this fact could be related to the different dispersion types of these two faunal groups: active for insects versus passive for crustaceans. Electronic supplementary material The online version of this article (doi:) contains supplementary material, which is available to authorized users. Guest editors: R. Céréghino, J. Biggs, B. Oertli & S. Declerck The ecology of European ponds: defining the characteristics of a neglected freshwater habitat     

Presence of three diapauses in a subtropical cockroach: control mechanisms and adaptive significance

Abstract.  Diapause is common among insects and is regarded as an adaptive response to periodic occurrence of adverse conditions. It occurs at a particular developmental stage, typically only once in a lifetime. However, little is known about the details of the control mechanism of life cycles with multiple diapauses in insects. In this study, a complex 2-year life cycle with three types of diapause is reported in a subtropical cockroach, Symploce japonica : a winter diapause in mid-nymphal instars, a summer diapause in later nymphal instars, and a reproductive diapause is reported in the adult stage. Nymphal development was extremely slow either at short days (winter diapause) or long days (summer diapause). Nymphs in summer diapause matured rapidly when transferred from long days to short days, indicating that seasonal changes in day-length are the pivotal factor in the control of this life cycle. It is proposed that the main significance of winter diapause in this subtropical species is to enable the nymphs to survive the mild winter successfully with reduced energy demand, and that of summer diapause is to delay adult emergence until late in the autumn for successful induction of the following adult diapause. Adults do not emerge until shortly before winter, yet the presence of diapause in the adult stage does not simply appear to be a response to cope with the winter conditions but, instead, ensures that reproduction will occur early the next year, before summer, because reproduction is greatly hampered at high temperature.     

Embryonic diapause is conserved across mammals

Embryonic diapause (ED) is a temporary arrest of embryo development and is characterized by delayed implantation in the uterus. ED occurs in blastocysts of less than 2% of mammalian species, including the mouse (Mus musculus). If ED were an evolutionarily conserved phenomenon, then it should be inducible in blastocysts of normally non-diapausing mammals, such as domestic species. To prove this hypothesis, we examined whether blastocysts from domestic sheep (Ovis aries) could enter into diapause following their transfer into mouse uteri in which diapause conditions were induced. Sheep blastocysts entered into diapause, as demonstrated by growth arrest, viability maintenance and their ED-specific pattern of gene expression. Seven days after transfer, diapausing ovine blastocysts were able to resume growth in vitro and, after transfer to surrogate ewe recipients, to develop into normal lambs. The finding that non-diapausing ovine embryos can enter into diapause implies that this phenomenon is phylogenetically conserved and not secondarily acquired by embryos of diapausing species. Our study questions the current model of independent evolution of ED in different mammalian orders.     

The evolution and maintenance of delayed implantation in the mustelidae (mammalia: carnivora)

Diapause, the temporary cessation of development at an early life-history stage, is widespread among animals and plants. The range of taxa exhibiting various forms of diapause indicates its enormous ecological significance and highlights its value as a model for examining life-history trait evolution. However, despite the impact of diapause on species ecology, there is little understanding of its adaptive value in many groups. Furthermore, the relative roles of phylogeny and ecology in determining the contemporary expression of the trait remain unresolved. Delayed implantation (DI) is a type of diapause found in several orders of mammals. It is particularly prevalent in the Mustelidae, with mustelids making up more than half of all mammals known to exhibit DI. This taxon is thus ideal for examining life-history predictors of DI and investigating the mode of evolution. Both maximum likelihood and maximum parsimony methods of ancestral state reconstruction indicated DI to be plesiomorphic in the mustelids, although multiple state changes are required to explain its contemporary distribution. After controlling for phylogeny, species with and without DI could be discriminated using just three variables: longevity, maximum latitude of the geographical distribution, and a term describing maternal investment. Our analyses supported the hypothesis that DI is more prevalent in seasonal climates. We also showed that longer-lived species are more likely to exhibit DI, suggesting a time cost to the trait. We found no correlate for the highly variable duration of DI, which remains unexplained. Although ecological factors can predict the distribution of DI in modern mustelids, phylogenetic constraint is likely to play an important role.     

Long life cycles in insects

Long life cycles covering more than one year are known for all orders of insects. There are different mechanisms of prolongation of the life cycle: (1) slow larval development; (2) prolongation of the adult stage with several reproduction periods; (3) prolongation of diapause; (4) combination of these mechanisms in one life cycle. Lasting suboptimal conditions (such as low temperature, low quality of food or instability of food resources, natural enemies, etc.) tend to prolong life cycles of all individuals in a population. In this case, the larvae feed and develop for longer than a year, and the active periods are interrupted by dormancy periods. The nature of this dormancy is unknown: in some cases it appears to be simple quiescence, in others it has been experimentally shown to be a true diapause. Induction and termination of these repeated dormancy states are controlled by different environmental cues, the day-length being the principal one as in the case of the annual diapause. The long life cycles resulting from prolonged adult lifespan were experimentally studied mainly in beetles and true bugs. The possibility of repeated diapause and several periods of reproductive activity is related to the fact that the adults remain sensitive to day length, which is the main environmental cue controlling their alternative physiological states (reproduction vs. diapause). Habitats with unpredictable environmental changes stimulate some individuals in a population to extend their life cycles by prolonged diapause. The properties of this diapause are poorly understood, but results of studies of a few species suggest that this physiological state differs from the true annual diapause in deeper suppression of metabolism. Induction and intensity of prolonged diapause in some species appear to be genetically controlled, so that the duration of prolonged diapause varies among individuals in a group, even that of sibles reared under identical conditions. Thus, long life cycles are realized due to the ability of insects to interrupt activity repeatedly and enter dormancy. This provides high resistance to various environmental factors. Regardless of the nature of this dormancy (quiescence, annual or prolonged diapause, or other forms) and the life cycle duration, the adults always appear synchronously after dormancy in the nature. The only feasible explanation of this is the presence of a special synchronizing mechanism, most likely both exo- and endogenous, since the adults appear not only synchronously but also in the period best suited for reproduction. As a whole, the long life cycles resulting from various structural modifications of the annual life cycle, are typical of the species living under stable suboptimal conditions when the pressure of individual environmental factors is close to the tolerance limits of the species, even though it represents its norm of existence. Such life cycles are also typical of the insects living in unstable environments with unpredictable variability of conditions, those developing in cones and galls, feeding on flowers, seeds, or fruits with limited periods of availability, those associated with the plant species with irregular patterns of blossoming and fruiting, and those consuming low-quality food or depending on unpredictable food sources (e.g., predators or parasites). Long cycles are more common in: (1) insect species at high latitudes and mountain landscapes where the vegetation season is short and unstable; (2) species living in deserts or arid areas where precipitation is unstable and often insufficient for survival of food plants; (3) inhabitants of cold and temporary water bodies that are not filled with water every year. At the same time, long life cycles sometimes occur in insects from other climatic zones as well. It is also important to note that while there is a large body of literature dealing with the long life cycles in insects, it mostly focuses on external aspects of the phenomenon. Experimental studies are needed to understand this phenomenon, first of all the nature of dormancy and mechanisms of synchronization of adult emergence.     

黄渤海甲壳类的分类多样性

为了解黄渤海甲壳类的分类多样性特征, 我们统计了2010-2015年中国水产科学研究院黄海水产研究所调查捕获的黄渤海甲壳类(软甲纲: 十足目与口足目)物种名录。结合历史文献, 进一步系统整理得到黄渤海甲壳类物种总名录。基于这2个名录, 应用分类阶元包含指数(the inclusion index at taxonomic level, TINCL_i)、平均分类差异指数(average taxonomic distinctness index, Δ⁺)和分类差异变异指数(variation in taxonomic distinctness index, Λ⁺)研究了其分类多样性特征。结果显示: 2010-2015年调查名录中, 甲壳类共93种, 隶属于2目39科66属, 其中10种为新分布种; 对虾科、藻虾科、长臂虾科、梭子蟹科和弓蟹科的物种数最多, 合计占总物种数的38.71%; TINCL_i分别为1.41种/属和2.38种/科; Δ⁺和Λ⁺分别为50.25和35.20。总名录中, 甲壳类共228种, 隶属于2目53科123属, 其中藻虾科、豆蟹科、对虾科、弓蟹科和鼓虾科的物种数最多, 合计占总物种数的30.70%; TINCL_i分别为1.85种/属和4.30种/科, Δ⁺和Λ⁺分别为50.18和30.87。对虾科的相对丰富度指数(the relative richness index, R_r)最高(100), 其次是梭子蟹科(71.43)和长臂虾科(62.50), 豆蟹科最低(6.25)。黄渤海甲壳类的平均分类差异指数(Δ⁺)明显小于鱼类(P < 0.05)。2010-2015年调查的Δ⁺计算值高于理论值, 且在理论值的95%置信区间内, 说明黄渤海甲壳类群落正处在中等程度的干扰中。     

昆虫延长滞育的研究

持续时间达1年以上的滞育,称为延长滞育,延长滞育的诱导、维持、解除均不同于简单滞育(滞育期短于1年)。本论文系统阐述了昆虫延长滞育的类型、滞育诱导及解除的环境因子、延长滞育物候学和生物学特性,延长滞育的遗传学及延长滞育的生态学意义。延长滞育是昆虫生活史的重要组成部分,是一种普遍现象。     

Physical and physiological factors in diapause initiation of two hyperparasites of the tobacco hornworm,Manduca sexta

Hypopteromalus tabacum diapauses as a last larval instar and Catolaccus aeneoviridis as a non-pharate pupa within cocoons of the primary parasite, Apanteles congregatus. Four factors (photoperiod, temperature, maternal age, and physiological state of the host) were tested for their significance in diapause initiation of both species. A 10L : 14D photoperiod produced a higher incidence of diapausing individuals than a 13L : 11D photoperiod. In the temperature range from 18 to 24°C, the incidence of diapause was inversely related to temperature. The incidence of progeny entering diapause varied with the age of the mother, younger ones producing fewer diapausing offspring. An increase in the number of C. aeneoviridis entering diapause was observed when the host, A. congregatus, was in the diapausing, rather than the nondiapausing condition. Analysis of the data indicated that interactions between these four factors also played an important rôle in diapause initiation of both species.     

Diapause incidence of progeny in relation to parental geographic origin,host plant and rearing density in the cabbage beetle,Colaphellus bowringi

The cabbage beetle, Colaphellus bowringi Baly (Coleoptera: Chrysomelidae), which is widely distributed in China, undergoes an imaginal diapause in the soil. In this study, we investigated the influences of parental geographic origin, host plant, and rearing density on the diapause incidence of progeny in this beetle. In studies conducted at 25 °C and L12:D12 photoperiod, the proportions of adults entering diapause were significantly different among latitudes from which the parents had been collected. The incidence of diapause increased with increasing latitude. Reciprocal cross tests between post‐diapause adults from different latitudes showed that there were significant differences in diapause incidence between pure‐bred and hybrid adults, suggesting that diapause incidence among progeny was determined by both the female and male, although the female appeared to have a stronger effect than the male. These results revealed that parental origin has an important influence on progeny diapause. Parental host plant species not only affected diapause incidence of the current generation, but also affected the incidence of diapause in the progeny produced by the non‐diapause parents; yet, the parental host plant had no influence on the incidence of diapause in the progeny produced by the post‐diapause parents. Rearing density of the parental generation had no significant effect on the incidence of diapause in the progeny.     

Trade-offs between storage and survival affect diapause timing in capital breeders

Many organisms spend the unfavourable part of the year, such as the winter season, in diapause or dormancy and reproduce in spring shortly after emergence. Reserves are acquired prior to diapause to cover metabolic costs and in some species also reproduction (capital breeding) directly after diapause. Storage is then a component of future reproduction, and capital breeders consequently pay a pre-breeding cost of reproduction as they risk dying while obtaining and carrying the reserves. How large should the reserves be, and to what extent should optimal storage, and thereby timing of diapause, depend on predation risk and reproductive strategy? We present a general and simplistic life history model of an arthropod (e.g. crustaceans or insects) that is exposed to background mortality risk when it accumulates reserves before diapause. The model optimizes diapause timing and resultant reserves for income, mixed and capital breeders, and predicts how mortality risk affects the degree of capital breeding. For income breeders, timing of diapause is insensitive to the risk while obtaining reserves as they, regardless of risk, acquire the minimum amount needed to survive the winter. For capital breeders, the higher the risk the earlier the diapause and less is consequently stored. Mixed breeders diapause late and store as much as pure capital breeders when exposed to low risk, but behave as income breeders and diapause early when mortality is high. Our model shows that the degree of capital breeding impacts phenology of diapause in a risk-dependent manner. This prediction should impact how diapause timing is thought of across a wide range of taxa, including the much studied marine copepods. Timing of diapause, including triggers and cues, can only be understood when the diversity of reproductive strategies and the adaptive value of storage is taken into account.     

中华稻蝗不同地理种群杂交子代的滞育率

为弄清中华稻蝗Oxya chinensis Thunberg卵滞育的遗传特征,调查中华稻蝗济宁、泗洪及株洲3个地理种群卵滞育的地理变异及亲本对杂交子代滞育的影响。结果表明:南方的株洲种群仅部分卵进入滞育,滞育率较低,而纬度较高的济宁、泗洪种群的卵滞育率达100%。说明不同地理种群的中华稻蝗卵滞育率存在着地理变异。将完全滞育的济宁、泗洪种群与滞育率较低的株洲种群的雌雄成虫进行正反杂交,济宁与株洲种群、泗洪与株洲种群的子代均有部分卵为非滞育卵,与株洲种群的滞育特征相似。但不管是以株洲种群为父本,还是为母本,杂交子代的滞育率均显著高于株洲种群,而与完全滞育的济宁、泗洪种群更为接近,说明中华稻蝗卵滞育的发生受雌雄基因的共同作用,但滞育程度与滞育率高的亲本的关联性更大。     

Geographic variation of reproductive diapause in the Drosophila auraria complex (Diptera: Drosophilidae)

ABSTRACT. In the Drosophila auraria complex (D. auraria Peng, D. biauraria Bock & Wheeler, D. triauraria Bock & Wheeler, D. quadraria Bock & Wheeler and D. subauraria Kimura), D. triauraria from the island of Yaku (30.3N in latitude) and D. quadraria from Taiwan (24.1N) had no or weak diapause, while strains of all the four species from the main islands of Japan had a firm reproductive diapause. These strains entered diapause at short daylengths and the critical daylength was longer and the incidence of diapause higher at a low rather than high temperature. In each species, the critical daylength was longer in strains from higher latitudes. Among sympatric populations of different species, D. subauraria always had the longest critical daylength, while D. auraria had the shortest one. The populations of D. biauraria and D. triauraria had longer critical daylengths than the sympatric populations of D. auraria , but this difference became smaller northwards. Since a longer critical daylength induces diapause earlier in autumn, D. subauraria would enter diapause earliest among these species, and D. auraria would do so latest. The late start of diapause in D. auraria may be related to its adaptation to domestic environments. On the other hand, the adaptive significance of the late start of diapause in northern populations of D. biauraria and D. triauraria is not clear.     

Stages of embryonic development in the amphipod crustacean, Parhyale hawaiensis

Studying the relationship between development and evolution and its role in the generation of biological diversity has been reinvigorated by new techniques in genetics and molecular biology. However, exploiting these techniques to examine the evolution of development requires that a great deal of detail be known regarding the embryonic development of multiple species studied in a phylogenetic context. Crustaceans are an enormously successful group of arthropods and extant species demonstrate a wide diversity of morphologies and life histories. One of the most speciose orders within the Crustacea is the Amphipoda. The embryonic development of a new crustacean model system, the amphipod Parhyale hawaiensis, is described in a series of discrete stages easily identified by examination of living animals and the use of commonly available molecular markers on fixed specimens. Complete embryogenesis occurs in 250 h at 26 degrees C and has been divided into 30 stages. This staging data will facilitate comparative analyses of embryonic development among crustaceans in particular, as well as between different arthropod groups. In addition, several aspects of Parhyale embryonic development make this species particularly suitable for a broad range of experimental manipulations.