Univoltine and bivoltine life cycles in insects: A model with density-dependent selection

Selection for univoltine and bivoltine life cycles in insects under resource-limited but favourable temperature conditions is analyzed with a difference equation model including density-dependent population dynamics based on the conceptual framework of an evolutionarily stable strategy. The model predicts that the bivoltine type can spread in a univoltine population when the fraction of density-independent rate of annual increase by producing a second generation exceeds the survival rate during diapause of the univoltine type, but monopoly of the bivoltine type is not possible unless it attains an equilibrium population density exceeding that of the univoltine type. The applicability of the model prediction in explaining the occurrence of a partial bivoltine cycle in predominantly univoltine population in the temperate zones is discussed.     

Asynchronous pupation of univoltine insects as evolutionarily stable phenology

Evolutionarily stable seasonal timing of larval feeding stages is studied theoretically for univoltine insects. In the evolutionarily stable (or ESS) population, each individual maximizes its own lifetime reproductive success by choosing the hatching and pupation dates, given the resource availability curve with a peak in the middle of a year, a higher daily mortality in the feeding stages, and the growth rate decreasing with the larval biomass in the population. If growth rate is proportional to the body size, the population at the ESS is composed of a mixture of phenotypes differing in hatching and pupation, but pupation interval over which some popation occur every day is much longer than hatching interval. If growth rate increases with the body size at a speed slower than linearly, large sized larvae should pupate earlier than small ones.     

Temperature- and density-dependence of diapause induction and its life history correlates in the geometrid moth Chiasmia clathrata (Lepidoptera: Geometridae)

The relative roles of genetics and developmental plasticity in creating phenotypes adapted to prevailing conditions are insufficiently understood. In potentially multivoltine temperate insects, individuals that do not enter diapause but develop directly into reproductive adults within the same season are severely time-constrained. Direct development is, however, under selection only if expressed in the wild. Thus, adaptive correlates of the direct development are expected to evolve and persist only in multivoltine populations. We studied the genetic and phenotypic components of variation in juvenile development in the geometrid moth Chiasmia clathrata from univoltine and bivoltine regions. Larvae were reared at two temperatures (14/20 °C) and densities (low/high) in a factorial split-brood experiment. High temperature and low density promoted direct development, the former condition being associated with a short development time, high growth rate and large body size. Genotypes of bivoltine origin had a higher propensity for direct development and seemingly expressed an exaggerated plastic response to increasing temperature compared to the ones from univoltine populations. Alternative life history phenotypes associated with the induced developmental pathway emerged only in the bivoltine region, direct development resulting in a short larval period, high growth rate and small size at 20 °C there. The degree of differentiation between the developmental pathways was insensitive to larval density; high density only decreased both development time and body size to a certain degree. We conclude that the differences between the pathways are not due to the induction of a particular pathway itself, but geographically varying selection pressures shape the correlation structure among life history traits and their pathway-specific expression.     

A population model for diapausing multivoltine insects under asymmetric cannibalism

Pupa-eating cannibalism occurs naturally in several insect species. Byasa alcinous is a multivoltine species of Red-bodied Swallowtail butterfly found in East Asia, which diapauses as pupa over the winter and whose larvae cannibalize eggs and pupae. We investigate the effects on population dynamics of increasing the asymmetric cannibalistic attack rate of a general insect species in different environmental conditions. We do this by theoretically formulating a generalized system of univoltine and bivoltine larvae over two generations in the spring and summer months. We predict that a lack of resources over the summer can force the population to become entirely univoltine, unless the second-generation bivoltine larvae increase their cannibalistic attack rate, and consume the diapausing pupae from the first generation. The model shows that under extreme environmental conditions, the persistence of univoltine larvae is favoured when faced with the threat of extinction. The model also predicts the conditions for the coexistence of both univoltine and bivoltine larvae, and the degree to which they can both coexist, which decreases as the resource in the second generation increases. This work provides the grounding for future theoretical and experimental consideration of the role of cannibalism in determining insect voltinism.     

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.     

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.     

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.     

Typology of life cycles of ground beetles (Coleoptera,Carabidae) in Western Palaearctic

An original classification of the life cycles of ground beetles from Western Palaearctic is proposed. The classification is based on a combination of five criteria: duration, number of generations per season, phenology of reproduction, stability, and repeatability of reproduction. According to the individual lifespan, the cycles are subdivided into annual and biennial ones. The annual life cycles may be uni-and bivoltine, whereas biennial ones are always univoltine. By the time of reproduction, winter-spring, spring, spring-summer, early summer, summer, late summer, summer-autumnal, autumnal, autumn-winter, winter, and aseasonal species are distinguished. The biennial and bivoltine cycles may be of both facultative and obligate nature. Species living only one season and having a continuous reproductive period are designated as semelparous, while those breeding during two or more years or having several distinct periods of reproduction in one season, as iteroparous. By now, 30 variants of life cycles in Carabidae from western Palaearctic have been established. Repeated similarly directed modifications of the life cycle may produce essentially different seasonal rhythms in some individuals. In this case, two subpopulation groups usually appear within the population. Under the most unfavorable conditions, these groups become practically isolated and hibernate at different ontogenetic stages. The individual development in each of these groups takes two years with the same seasonal rhythm. Among the types considered, only obligate-bivoltine life cycles are always polyvariant, but annual univoltine and obligate-biennial ones are always univariant. The facultative-bivoltine and biennial life cycles may be realized as uni-and polyvariant ones, depending on the environmental conditions.     

Life-history strategies and production of Tinodes waeneri (L.) (Trichoptera) in Lake Esrom,Denmark

The life cycle and production of Tinodes waeneri (L.) was examined at five shallow littoral localities in Lake Esrom, Denmark, during 1979/80. Five larval instars were demonstrated. The differences in temporal composition of instars indicated three different life cycles. A bivoltine strategy was shown for the most exposed locality which also had the highest average abundance equal to 11 500 ind. m^–2. A univoltine population was found in the more sheltered NW part of the lake with an average density of 1 500 ind. m^–2. At the three remaining stations the life cycles were partly bivoltine with wintering populations of mixed cohorts and densities between 10 500 and 3 000 ind. m^–3. Two distinct flight periods with maxima in June and August were demonstrated for bi- and partly bivoltine populations. Differences in rates of growth and elimination added to the variability in life cycle. Growth rates peaked in August (5.0–7.4% d^–1) at an average temperature of 20°C. Estimates of production ranged from 1.9 to 17.5 g AFDW m^–2 a^–1 with an average of 8.0 g AFDW m^–2. The P/B ratios, which were within the expected range for uni- and bivoltine populations of trichopterans, were 5.73 for the bivoltine population and 3.31 for the univoltine population.Estimates of consumption revealed that the populations could be sustained by autochthonous epilithic production in the habitats. Variability in the quality and seasonal availability of food were judged to influence the type of life cycle.Lake Esrom Littoral Research Publ. No. 8. Publication No. 385 from the Freshwater Biological Laboratory, University of Copenhagen, 51, Helsingørsgade, DK-3400 Hillerød, Denmark.Lake Esrom Littoral Research Publ. No. 8. Publication No. 385 from the Freshwater Biological Laboratory, University of Copenhagen, 51, Helsingørsgade, DK-3400 Hillerød, Denmark.     

Alternative life histories in the water strider Gerris lacustris: time constraint on wing morph and voltinism

The wing dimorphic water strider Gerris lacustris L. (Heteroptera: Gerridae) switches to a bivoltine life cycle under favorable climatic conditions. The switch in voltinism is accompanied by a reduction of wing development in the directly reproducing midsummer generation, while the diapausing generation has a high fraction of long‐winged individuals. We investigated whether the thermal energy (degree‐days) available in natural habitats constrains the combination of developmental pathway and wing morph. Offspring of G. lacustris were reared under quasi‐natural conditions at two temperature regimes to determine the thermal constant k required to complete adult development in either wing morph. The thermal constant for egg‐to‐adult development of the short‐winged morph was about 20% lower than of the long‐winged morph. Based on the results from the outdoor laboratory experiment, we calculated the total degree‐days necessary to complete the possible combinations of wing morph pattern and voltinism. Comparison of these estimates with the thermal energy actually available during the reproductive season of 2004 for various natural habitats (sun‐exposed field ponds and shaded forest ponds) suggests that voltinism as well as wing morph pattern is strongly limited by the number of degree‐days available in these habitats. On forest ponds, only univoltine life cycles were possible, whereas on field ponds temperature allowed bivoltine life cycles. However, only the eggs laid at the very beginning of the season had the potential to accumulate enough degree‐days to complete a bivoltine life cycle with both generations long‐winged. We conclude that thermal energy is the main environmental constraint limiting voltinism of populations in the two habitat types. Furthermore, the available thermal energy also seems to influence the determination of the seasonal wing pattern in G. lacustris.     

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.     

Experiments on the effects of food and density on voltinism in a stream-dwelling water strider (Aquarius remigis)

1. The stream water strider Aquarius remigis shows a latitudinal pattern of variation in voltinism. In general, populations with shorter growing seasons (e.g. in eastern Canada) tend to be univoltine (animals that reach adulthood in the summer overwinter before reproducing in the following spring), whereas populations with somewhat longer growing seasons (e.g. in the north-eastern United States) tend to be bivoltine. 2. This pattern was broken at our study site in the south-eastern United States (Kentucky) where A. remigis had a long growing season, but was almost always univoltine. In summer 1993, however, adult A. remigis in central Kentucky displayed a bivoltine reproductive cycle; i.e. individuals in some pools began breeding shortly after maturing to the adult stage. 3. A field survey documented a negative relationship between local water strider density and reproductive activity in prediapause adults. A laboratory experiment manipulating food availability and density, revealed that animals held at low density with high food levels displayed greater mating activity and egg production than did their counterparts at higher density or lower food levels. 4. A laboratory experiment also showed that high water strider density resulted in a greater frequency of very short pair durations (< 10 min). 5. Although the observed effects of density and food availability on mating activity of prediapause adults seem intuitively reasonable, they differ from the patterns observed in overwintered adults. The difference in reproduction patterns might be due to differences in selective pressures on prediapause vs. post-diapause adults.     

Life-history and sex allocation in Trypoxylon (syn. Trypargilum) lactitarse (Hymenoptera; Crabronidae)

Hymenopterans have become a model for the study of factors that govern sex allocation. In 1983, Seger proposed a model to study Sphecidae wasps with a strong prediction that sex ratio for univoltine wasps should be 1 : 1 (female : male), and for partially bivoltine species it should be male-biased. The present study investigates if Trypoxylon lactitarse (Saussure, 1867) is a univoltine or a bivoltine species and if Seger's model prediction fits the pattern of sex ratio found in this species. The study was carried out at Parque Municipal das Araucárias, in the municipality of Guarapuava, state of Paraná, southern Brazil, from December 2001 to December 2004. Nests of T. lactitarse were obtained using trap-nests drilled longitudinally to a depth to 80 mm with 7.0, 10.0 and 13.0 mm opening diameter. They were placed in a very heterogeneous site filled with araucaria forests, swamps and grasslands. Trypoxylon lactitarse showed two alternative life histories: either they pupated immediately and emerged as adults later in the same season (direct development), or they entered diapause, overwintering and pupating the following spring (delayed development). Its annual sex ratios were not significantly different from 1 : 1, and both sex ratio of overwintering and sex ratio of direct-developing wasps were also not significantly different from 1 : 1, in all years of this study. By examining these results, it was possible to conclude that although T. lactitarse is a multivoltine species, with four generations per year and two alternative life histories, its sex ratio did not support Seger's model.     

Climatic adaptation and species status in the lawn ground cricket

Summary The cricket tentatively identified as Pteronemobius taprobanensis shows a stepwise pattern of latitudinal variation in ovipositor length. Abrupt elongation of ovipositor at about 28° N marks the replacement of the subtropical form by the temperate form. The latter maintains almost a constant ovipositor length up to about 35° N within the bivoltine area. Further north in the univoltine area, an ascending cline extends to about 39° N, beyond which no further increase occurs. The ovipositor length adjusted for body size shows a northeastward increase in each of the univoltine and bivoltine areas, though this tendency is less clear in the latter. The optimum length of ovipositor would vary with the relative amounts of gain (due to the protection of eggs in the soil) and loss (due to the metabolic cost and the difficulty to emerge from the soil) in fitness. If so, it may be predicted that a longer ovipositor would be selected for, when the metabolic cost and the risk at hatching are smaller, the environmental pressure in the egg stage is stronger, and the egg stage lasts longer. The last parameter seems to be mainly responsible for the observed association of the type of life cycle with the geographic pattern of variation in ovipositor length.Contribution No. 76 from the Laboratory of Entomology, Hirosaki University     

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.     

Life cycles and habitats of wisconsin heptageniidae (ephemeroptera)

Detailed studies were made of the life cycles of Heptageniidae known to occur in Wisconsin. 19 species had univoltine cycles while two and possibly a third had bivoltine cycles. Three univoltine species developed in late spring and early summer while the other univoltine species developed in fall, winter and early spring. For three of the univoltine species, eggs hatched both in fall and the following spring. Diagrams of the life cycles of 15 Wisconsin heptageniids are presented, illustrating the different types of life cycles. Also presented are observation on the food and habitats of the nymphs and flight periods of the adults.     

Geographical variation in insect developmental period: effect of host plant phenology on the life cycle of the bruchid seed feeder shape Kytorhinus sharpianus

The voltinism of the bruchid Kytorhinus sharpianus Bridwell (Coleoptera: Bruchidae) and the phenology of its host plant Sophora flavescens Aiton (Leguminosae) were observed at four latitudes: Aomori (40°46' N), Obanazawa (38°37' N), Kujiranami (37°21' N) and Mitsuma (36°05' N) in northeastern Honshu (Japan). Kytorhinus sharpianus life cycle ranged from bivoltine and partially trivoltine in the south to univoltine and partially bivoltine in the north. Sophora flavescens started growing later in spring at higher latitudes. However, the relative growth rate was higher in the north (Aomori) than in the south (Mitsuma). In parallel with this, the first-generation of adult K. sharpianus appeared later at higher latitudes. When the four local populations were reared at 24 °C, L16:D8 and 65% r.h., males developed faster than females. The mean developmental time showed a saw-toothed latitudinal cline. The reversion in the latitudinal trend of variation corresponded to the change in the major type of life cycles from univoltine to bivoltine. Two heat units throughout the year and post-fruiting period were calculated as the sums of degree-days above the developmental threshold (12 °C) of K. sharpianus. Both heat units decreased in parallel with each other with increasing latitude. The greater growth rate of hosts in the northern population compensated for the smaller heat units. In addition, when the heat units were divided by the degree-days needed to complete development, the numerical value was the approximate number of generations observed in each locality.     

Ecological and genetic correlates of range expansion in Coenonympha tullia

Range expansion by the North American butterfly species Coenonympha tullia is associated with dramatic changes in life history and in genetic and morphological variation. Eight of ten independent, variable loci exhibit step-clines in allele frequency; step-clines also occur in four wing pattern characters. Populations from the old part of the range are univoltine, and have significantly less genetic and morphological variation than populations from the recently colonized ranger, which arc bivoltine. The concordance of life history with genetic and morphological variation suggests that differences between univoltine and bivoltine populations are maintained by selection. Increased electrophoretic variation in the recently colonized range may have arisen by selection on rare variants within the old part of the range.     

Resource utilization, overlap and temporal dynamics in a guild of mountain stream insects

SUMMARY 1. Resource utilization was quantified for six mayfly (Ephemeroptera) and one caddis (Trichoptera) species comprising a lotic scraper/collector-gatherer guild across three niche dimensions (temporal, trophic and spatial). Based on trophic differences and inferred microspatial utilization, the members of this guild separated into two groups: (1) cryptic detritivores and (2) exposed algivores.
2. Each species demonstrated a slow seasonal univoltine life cycle except for Epeorus longimanus (Eaton) and Baetis iricaudatus (Dodds) which were fast seasonal univoltine and multivoltine, respectively.
3. Temporal sequencing of periods of peak resource utilization were not demonstrated by the members of this guild. A null analysis indicated that periods of peak resource utilization were aggregated.     

Seasonal changes in a cactus‐hoverfly (Diptera: Syrphidae) network

1. We analysed a cacti‐syrphid community focusing on the exploitation of decaying cacti resources by the flies, i.e. if exploitation exhibited a nested topology as a structural pattern, or whether it was temporally random. If availability of cactus resources was predictable during the rainy season, it would then be exploited by a more structured community, or as resource availability would be unpredictable during the dry season, we should expect it to be exploited by a random community. 2. We registered 12 Copestylum species (9 in dry and 11 in rainy season). Four cactus species were recorded per season, three were shared between seasons. 3. The community of Copestylum larvae in the rainy season was not randomly assembled but highly nested, revealing a highly structured pattern of resource use. It exhibited a random organization for the dry season. The high nestedness value obtained for the rainy season suggests that factors along with competition must play a major role in determining community structure. 4. Succession in the cacti‐syrphid community mediated by microorganisms involved in necrosis is an important factor structuring nested subsets. The studied networks were small, which may limit the power of the analysis, and strong conclusions could also be limited.