Latitudinal clines in the timing and temperature-sensitivity of photoperiodic reproductive diapause in Drosophila montana

Reproductive diapause is a primary mechanism used by arthropods to synchronize their life cycle with seasonal changes in temperate regions. Our study species, Drosophila montana, represents the northern insect species where flies enter reproductive diapause under short day conditions and where the precise timing of diapause is crucial for both survival and offspring production. We have studied clinal variation in the critical day length for female diapause induction (CDL) and their overall susceptibility to enter diapause (diapause incidence), as well as the temperature sensitivity of these traits. The study was performed using multiple strains from four latitudinal clines of the species – short clines in Finland and Alaska and long clines in the Rocky Mountains and the western coast of North America – and from one population in Kamchatka, Russia. CDL showed strong latitudinal clines on both continents, decreasing by one hour per five degrees decline in latitude, on average. CDL also decreased in all populations along with an increase in fly rearing temperature postponing the diapause to later calendar time, the effects of temperature being stronger in southern than in northern population. Female diapause incidence was close to 100% under short day/low temperature conditions in all populations, but decreased below 50% even under short days in 19°C in the southern North American western coast populations and in 22°C in most populations. Comparing a diversity of climatic data for the studied populations showed that while CDL is under a tight photoperiodic regulation linked with latitude, its length depends also on climatic factors determining the growing season length. Overall, the study deepens our understanding of how spatial and environmental parameters affect the seasonal timing of an important biological event, reproductive diapause and helps to estimate the evolutionary potential of insect populations to survive in changing climatic conditions.     

Rapid adaptive evolution of the diapause program during range expansion of an invasive mosquito

In temperate climates, the recurring seasonal exigencies of winter represent a fundamental physiological challenge for a wide range of organisms. In response, many temperate insects enter diapause, an alternative developmental program, including developmental arrest, that allows organisms to synchronize their life cycle with seasonal environmental variation. Geographic variation in diapause phenology contributing to local climatic adaptation is well documented. However, few studies have examined how the rapid evolution of a suite of traits expressed across the diapause program may contribute to climatic adaptation on a contemporary timescale. Here, we investigate the evolution of the diapause program over the past 35 years by leveraging a “natural experiment” presented by the recent invasion of the Asian tiger mosquito, Aedes albopictus, across the eastern United States. We sampled populations from two distinct climatic regions separated by 6° of latitude (∼700 km). Using common-garden experiments, we identified regional genetic divergence in diapause-associated cold tolerance, diapause duration, and postdiapause starvation tolerance. We also found regional divergence in nondiapause thermal performance. In contrast, we observed minimal regional divergence in nondiapause larval growth traits and at neutral molecular marker loci. Our results demonstrate rapid evolution of the diapause program and imply strong selection caused by differences in winter conditions.     

Effect of temperature on queen oviposition and seasonal colony development in <Emphasis Type="Italic">Lasius japonicus</Emphasis> (Hymenoptera: Formicidae)

Although day length plays a critical role in the seasonal development of many temperate insects, this study showed that this variable is less important than temperature for seasonal regulation of an ant’s life cycle. Here, we examined the effects of temperature on queen oviposition and seasonal colony development of Lasius japonicus Santschi. Queens were collected soon after their nuptial flight and were reared under constant laboratory conditions; colony development was analyzed. The percentage of larvae- and pupae-emerged colonies was reduced in low rearing temperatures, indicating that temperature is the primary environmental factor for the regulation of seasonal development. Larval diapause was induced at higher temperatures than the reproductive diapause of queens. Larvae need to enter diapause before winter; nevertheless, eggs that were still unhatched in late autumn would not necessarily be wasted because they could be eaten by queens. Cyclic fluctuation in the egg number was observed. At 25 °C, the second increase in egg number was synchronized with pupation, suggesting a social effect on queen oviposition. In contrast, at 20 and 17.5 °C, the clear second peak of oviposition was found in colonies wherein larvae did not emerge, suggesting that endogenous rhythmicity is involved in the regulation of queen oviposition.     

Geographic variation in diapause induction under constant and changing conditions in Helicoverpa armigera

Variation in the incidence of diapause in local populations of Helicoverpa armigera (Hübner) and Helicoverpa assulta (Guenée) (Lepidoptera: Noctuidae) was examined in relation to changes in photoperiod and/or temperature during the larval period. Temperate zone populations of H. assulta, a native species in temperate Japan, showed a high incidence of diapause induction when only the photoperiod was decreased during the larval period, even at favorable temperatures. This photoperiod‐dependent response may allow H. assulta to foresee the beginning of autumn well in advance in the temperate zone, where temperature conditions are severe. In contrast, temperate zone populations of H. armigera, an invasive and polyphagous species mainly distributed in the subtropics, showed a high incidence of diapause only when both photoperiod and temperature decreased, whereas subtropical populations showed a very low incidence of diapause under the same conditions. Furthermore, both temperate zone and subtropical populations of H. armigera enter diapause under constant low temperatures at short‐day photoperiod. Thus, there is geographic variation in sensitivity to diapause‐inducing stimuli (changes in photoperiod and temperature) in H. armigera. This variation may be a part of the climatic adaptation achieved by H. armigera in Japan.     

Coexistence of similar genotypes of Daphnia magna in intermittent populations: response to thermal stress

We investigated the diversity and thermal response of a fitness related trait, juvenile growth rate, in seasonal population samples of Daphnia magna from two temperate ponds. Both populations were intermittent, i.e. they disappeared from the water body and recolonized seasonally by hatching from resting eggs in the sediment.
Temporally isolated clones of Daphnia magna showed the typical asymmetric response for growth rate with temperature and a sharp decline after the maximum response at 26°C (TMR). There was no evidence for genetically adapted seasonal groups. Despite significant genetic variation among clones and for phenotypic plasticity (G×E interactions without genetic correlations), seasonal groups of clones showed no shift in TMR and mean temperature reaction norms were similar among groups and both populations. Heritabilities remained similar among temperatures despite a large increase in genetic variance at stressfully high temperatures of 29°C and 32°C, due to simultaneous increase in environmental variance. Further, heritabilities remained high among sample periods and were not eroded during several months of asexual reproduction.
Regular diapause, an intrinsic feature of intermittent Daphnia populations, may replace the need for physiological temperature adaptation and promote maintenance of diversity through phenotypic similarity by reducing the time over which competitive interactions occur. Such populations are unlikely to be directly affected by elevated temperatures. They have a large potential for phenotypic plasticity as their TMR is higher than the temperature normally encountered.     

Life-cycle regulation and life history plasticity in the speckled wood butterfly: are reaction norms predictable?

We investigated whether interpopulational variation in life-cycle regulation and life-history plasticity, in response to photoperiod, is predictable from considerations of what would be the adaptive life cycle and life history in a given environment. The investigation was performed on five populations of the speckled wood butterfly, Pararge aegeria (L.) (Lepidoptera: Nymphalidae), from central and south Sweden, England, Spain and Madeira. Insects from all five populations were reared at all daylengths from 10 h to 20 h at 17^oC. Larval and pupal development times were noted. Predictions were met regarding the type of life-cycle regulation and the shape of reaction norms. Evidence for diapause (larval summer and winter diapause, pupal winter diapause) was found in the three northern populations (P. a. tircis) but not in the two southern populations (P. a. aegeria). Photoperiodic thresholds for diapause induction followed the predicted latitudinal patterns, and this was also the case regarding quantitative regulation of development time (by photoperiod) among directly developing individuals. Under direct development, development time was progressively shorter in shorter daylengms in the two Swedish populations, where this signals progressively later dates. This was not found in the English, Spanish and Madeiran populations where such a response is likely to be maladaptive, because one or more generations of larvae are present before summer solstice. There were also unexpected results, for which we propose preliminary adaptive explanations.     

Seasonal plasticity in growth and development of the speckled wood butterfly, Pararge aegeria (Satyrinae)

Regulation of growth and development by photoperiod was studied in a population of the speckled wood butterfly, Purarge aegeria L. (Lepidoptera: Satyrinae), from southern Sweden. Individuals were reared in a range of photoperiodic regimes (9L. to 22L) and temperatures (13°C to 21° C). Plasticity was found for important life-history traits- generation time, growth rate and final weight and seasonal regulation of development in response to photoperiod was found to occur at two levels. Purarge aegeria hibernates as a third instar larva or in the pupal stage, cantering one of four major developmental pathways in response to photoperiod: (1) direct development in both the larval and pupal stages, (2) pupal winter diapause with or (3) without a preceding larval summer diapause, or (4) larval winter diapause. In addition to this high-level regulation of individual development, larval growth rate and pupal development rate also appear to be finally regulated by photoperiod within each major pathway. As photoperiods decreased from 22 h to 17 h at 17° C, growth rate among directly developing larvae increased progressively, as was the case for larva? developing according to a univoltine life cycle from 17 h to 14 h. At two photoperiods, 13 h and 16 h (corresponding to shifts between major pathways), both larval and pupal development were extremely variable with the fastest individuals developing directly and the slowest developing with a diapause. This indicates a gradual nature of diapause itself, suggesting that the two level may not he fundamentally different.     

Adaptative significance of a temperature induced diapause in a cosmopolitan parasitoid of Drosophila

Abstract. 1. We have previously demonstrated pre-pupal diapause in a tropical population of Leptopilima boulardi Barbotin, Carton and Kelner-Pillault (Cynipidae, Hymenoptera), a larval parasitoid of Drosophila melanogaster Meigen. Prepupal diapause was induced by low temperature (17.5°C) but absent at 25°C; it was independent of photoperiod.
2. Four populations which originated from different latitudes (4°S to 44°N) exhibit the same response to temperature without any major genetic geographical variation.
3. In temperate areas, this diapause may permit a phenological and temporal coincidence between the parasitoid and its host whose larval growth is only possible for temperatures above 13°C.
4. The significance of the persistence of this diapause in tropical areas is discussed.     

The genetic architecture underlying diapause termination in a planktonic crustacean

Diapause is a feature of the life cycle of many invertebrates by which unfavourable environmental conditions can be outlived. The seasonal timing of diapause allows organisms to adapt to seasonal changes in habitat suitability and thus is key to their fitness. In the planktonic crustacean Daphnia, various cues can induce the production of diapause stages that are resistant to heat, drought or freezing and contain one to two embryos in developmental arrest. Daphnia is a keystone species of many freshwater ecosystems, where it acts as the main link between phytoplankton and higher trophic levels. The correct seasonal timing of diapause termination is essential to maintain trophic interactions and is achieved via a genetically based interpretation of environmental cues like photoperiod and temperature. Field monitoring and modelling studies raised concerns on whether populations can advance their seasonal release from diapause to advances in spring phenology under global change, or if a failure to adapt will cause trophic mismatches negatively affecting ecosystem functioning. Our capacity to understand and predict the evolution of diapause timing requires information about the genetic architecture underlying this trait. In this study, we identified eight quantitative trait loci (QTLs) and four epistatic interactions that together explained 66.5% of the variation in diapause termination in Daphnia magna using QTL mapping. Our results suggest that the most significant QTL is modulating diapause termination dependent on photoperiod and is involved in three of the four detected epistatic interactions. Candidate genes at this QTL could be identified through the integration with genome data and included the presynaptic active zone protein bruchpilot. Our findings contribute to understanding the genomic control of seasonal diapause timing in an ecological relevant species.     

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.     

Photoperiodic response in the subtropical and warm‐temperate zone populations of the southern green stink bug Nezara viridula: why does it not fit the common latitudinal trend?

The photoperiodic response of diapause induction is studied in females of five subtropical and warm‐temperate zone populations of Nezara viridula (L.) (Heteroptera: Pentatomidae) in Japan (26.4–34.7°N; 127.4–135.7°E). Laboratory tests at 25 °C demonstrate that both warm‐temperate and subtropical populations have pronounced photoperiodic responses of adult diapause induction. Under short‐day conditions (LD 10 : 14 h), 73–100% of females enter diapause, whereas, under long‐day conditions (LD 15 : 9 h), 87–100% of females are nondiapause and reproduce. When the critical photoperiod for diapause induction is plotted against the latitude of origin of each population, the data points do not show the expected tendency of increasing critical photoperiod northwards but, instead, vary between 12 h 15 min and 13 h 30 min. It is suggested that adults from different populations of such a highly migratory species move often among subtropical islands (by themselves or being assisted by typhoons), thus constantly destabilizing the photoperiodic responses. Although important for general synchronization of seasonal development in the tropics and subtropics, winter diapause might not be so critical for survival in mild winters in these zones. Such circumstances might make the selective pressure over the photoperiodic response less severe in the tropics and subtropics than in the temperate zone. It is suggested that the current climate warming might contribute to this situation as well by promoting polewards migrations and lessening the selective pressure of overwintering conditions.     

Temperature and photoperiodic control of diapase induction in the ant <Emphasis Type="Italic">Lepisiota semenovi</Emphasis> (Hymenoptera,formicidae) from Turkmenistan

The ants L. semenovi has been found to belong to species with endogenous-heterodynamic seasonal life cycles with the obligate diapause induced predominantly by factors internal for a colony, whereas external ecological factors (photoperiods and temperature) produce merely modifying effects by accelerating or delaying the diapause onset. The photoperiodic and temperature regulation of diapause induction in larvae and queens is shown. Under effect of short days and low temperature the periods of larval pupation and queen oviposition in a colony are shortened markedly, i.e., the diapause of larvae and queens occurs earlier. The daily rhythms of temperature 15/25°C and particularly 20/30°C as compared with constant temperatures 20 and 25°C that correspond to the mean circadian temperatures of the thermorhythm, inhibit manifestations of the short day effects by stimulating the non-diapause development and increasing duration of the seasonal development cycle of ant colonies. The L. semenovi photoperiodic reaction is quantitative, as development and pupation of larvae and egg-laying of queens cease sooner or later under both the short and the long days, but in the latter case significantly later. Thus L. semenovi is one more example among very rare ant species that are revealed to have the photoperiodic regulation of the colony development seasonal cycle.     

中华稻蝗长沙种群的生活史及其卵滞育的进化意义

中华稻蝗Oxya chinensis为重要的水稻害虫,在我国除青海、西藏、新疆、内蒙古等未见报道外,南起海南北至东北均有分布,在许多的分布区域1年发生1代。为探索中华稻蝗长沙种群的生活史及其季节适应特征,通过野外和实验室的研究,调查了其发生代数、孵化率和卵滞育率的季节变化及越冬卵的存活率。结果显示,中华稻蝗长沙种群为1年2代和1年1代混合发生:第1代卵产卵后大部分孵化为若虫而1年完成2代,但亦有19.4% -4.1%的卵不孵化而1年只能完成1世代。第1代成虫于6月上旬至8月上旬羽化,6月下旬至8月中旬产卵;第2代若虫于7月初开始孵化,9-10月羽化为成虫,10月上旬至11月下旬产卵。在室外自然条件下,中华稻蝗长沙种群6-8月(第1代)和10-11月(第2代)所产卵块均为部分滞育,滞育率为30%左右,皆无显著差异。然而,其卵滞育率在12月以后显著降低,仅为6.6%或以下,卵滞育快速地得以解除。因此,包括非滞育卵和滞育解除卵,中华稻蝗长沙种群的越冬卵皆以非滞育状态度过其后的寒冷季节。即使是遭遇长江流域2007年末至 2008年初异常寒冷的冬季,在长沙地区越冬后其卵的存活率亦在98%以上。非滞育状态的中华稻蝗长沙种群越冬卵完全能安全地越冬,其滞育的发生并非是为了提高其耐寒性而安全度过不适环境。并探讨了中华稻蝗长沙种群卵滞育的进化意义。     

Seasonal temperature alone can synchronize life cycles

In this paper we discuss the effects of yearly temperature variation on the development and seasonal occurrence of poikiliothermic organisms with multiple life stages. The study of voltinism in the mountain pine beetle (Dendroctonus ponderosae Hopkins), an important forest insect living in extreme temperature environments and exhibiting no diapause, provides a motivational example. Using a minimal model for the rates of aging it is shown that seasonal temperature variation and minimal stage-specific differences in rates of aging are sufficient to create stable uni-and multi-voltine oviposition cycles. In fact, these cycles are attracting and therefore provide an exogenous mechanism for synchronizing whole populations of organisms. Structural stability arguments are used to extend the results to more general life systems.     

Differences in haemolymph proteins in relation to diapause and wing dimorphism inPyrrhocoris apterus (L.) (Heteroptera: Pyrrhocoridae)

Three different cultures of dimorphic bug,Pyrrhocoris apterus, were analyzed concerning diapause and its relation to wing morph pattern. The proportion of macropterous bugs was considerably higher (36%) in the Mediterranean culture from Israel than that (1.3%) in the temperate culture from the Czech Republic. The macropterous morph- and brachypterous morphrelated types of reproduction arrest, differing by the length of pre-oviposition period, were distinguished in cultures analyzed. The reproduction arrest with an average pre-oviposition period of 38.2 days in Mediterranean macropters and 18.5 days in macropters from selected macropterous strain, was found to be typical for macropterous morph. Two different photoperiodic conditions induced macropterous morph-related reproduction arrest, the long-day (18 h light-6 h dark) photoperiod in macropterous strain macropters and the short-day (12 h light-12 h dark) photoperiod in Mediterranean macropters. The brachypterous morph-related reproduction arrest, characterized by pre-oviposition period longer than 90 days, occurred predominantly in diapausing brachypterous bugs. While the hibernal diapause of brachypterous bugs was characterized by a very high level of the 78- and 82-kDa proteins in haemolymph, their content in haemolymph of macropters during macropterous morph-related reproduction arrest was almost as low as in the reproductive adults. The variation of reproduction arrest in relation to wing dimorphism represents an important feature in the life strategy ofP. apterus.     

Time of the season: the effect of host photoperiodism on diapause induction in an insect herbivore,Leptinotarsa decemlineata

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The evolution of an annual life cycle in killifish: adaptation to ephemeral aquatic environments through embryonic diapause

An annual life cycle is characterized by growth, maturity, and reproduction condensed into a single, short season favourable to development, with production of embryos (seeds, cysts, or eggs) capable of surviving harsh conditions which juveniles or adults cannot tolerate. More typically associated with plants in desert environments, or temperate‐zone insects exposed to freezing winters, the evolution of an annual life cycle in vertebrates is fairly novel. Killifish, small sexually dimorphic fishes in the Order Cyprinodontiformes, have adapted to seasonally ephemeral water bodies across much of Africa and South America through the independent evolution of an annual life history. These annual killifish produce hardy desiccation‐resistant eggs that undergo diapause (developmental arrest) and remain buried in the soil for long periods when fish have perished due to the drying of their habitat. Killifish are found in aquatic habitats that span a continuum from permanent and stable to seasonal and variable, thus providing a useful system in which to piece together the evolutionary history of this life cycle using natural comparative variation. I first review adaptations for life in ephemeral aquatic environments in killifish, with particular emphasis on the evolution of embryonic diapause. I then bring together available evidence from a variety of approaches and provide a scenario for how this annual life cycle evolved. There are a number of features within Aplocheiloidei killifish including their inhabitation of marginal or edge aquatic habitat, their small size and rapid attainment of maturity, and egg properties that make them particularly well suited to the colonization of ephemeral waters.     

光周期和温度对亚洲玉米螟滞育诱导的影响

亚洲玉米螟Ostrinia furnacalis (Guenée)属兼性滞育昆虫, 其滞育特性与种群利用适生境的最大化和季节性活动密切相关。解析季节性因素如光周期和温度对其滞育的诱导作用可为预测种群发生动态提供科学依据。本实验在HPS 500型和HPG-320H型自动控制环境气候箱中, 测定了RH 80%下温度20℃, 27℃和30℃与11个光周期组合对吉林农安（NA）、 河北衡水（HS）、 广东惠州（HZ）和海南海口（HK）等4个地理种群的滞育诱导作用。结果表明： 光周期、 温度及其交互作用均对亚洲玉米螟滞育诱导具有重要影响, 其中光周期在滞育诱导中起主导作用。在20℃条件下, 其光周期反应曲线属典型的长日照反应型, 临界光周期随种群分布的地理纬度降低而缩短, 4个地理种群NA, HS, HZ和HK的临界日昼长依次为14 h 3 min, 13 h 59 min, 13 h 32 min和13 h 7 min, 最有效的滞育诱导光周期是日昼长12 h。另一方面, 随种群分布纬度升高, 其对光周期诱导滞育的敏感性降低。温度为27℃时, 其光周期反应曲线为短日照 长日照反应型, 各种群有两个临界光周期, 临界日昼长依次为12 h 50 min和13 h 32 min, 11 h 35 min和13 h 8 min, 12 h 58 min和13 h 1 min, 以及11 h 50 min和12 h 26 min, 且最有效的滞育诱导光周期范围的滞育率明显低于20℃。一定温度范围内（20℃～27℃）, 随温度升高, 临界光周期缩短; 温度达到30℃时则滞育显著被抑制, 滞育率仅为4.3%或更低。这些结果说明温度对亚洲玉米螟滞育的光周期诱导具有很强的补偿作用。因此, 在自然界亚洲玉米螟的滞育属具有温度补偿作用的长日照反应型昆虫, 临界光周期随地理纬度北移而增长; 种群滞育的短日照 长日照反应型特性可能是产生局部世代种群的重要内因。     

Seasonal adaptations of different geographical populations of the sunflower moth, Homoeosoma electellum

A photothermogram constructed for a central Missouri population (ca. 39°N latitude) of the sunflower moth, Homoeosoma electellum (Hulst) predicted that this population has a seasonal life cycle of 2 complete and a partial third generation per year, and that daylengths of less than 13 h 30 min light/day and mean temperatures of less than 20°C induce the mature larval diapause. A test of the predicted life cycle revealed that larvae entered diapause when they were exposed from their first instar onwards to natural conditions in central Missouri beginning September 15, 1982. Sunflower moths obtained from northwest Texas (ca. 35°N latitude) and northeast South Dakota (ca. 45°N latitude) displayed shorter critical photoperiods for diapause induction at 20°C (12 h 30 min light/day and 12 h 15 min light/day, respectively) than did those from Missouri. The population of the sunflower moth obtained from South Dakota does not, therefore, appear to be adapted to local conditions, and moths might disperse from lower latitudes to establish transiet populations each year.