Energy storage during reproductive diapause in the Drosophila melanogaster species group

Summary Temperate species of the Drosophila melanogaster group enter reproductive diapause for overwintering in response to short daylength. During the prediapause period they accumulate triacylglycerols, but not glycogen, as energy resources. The capacity for storing triacylglycerols differs between species, and appears to be closely correlated with diapause and cold-hardiness; cool-temperate species, such as those of the auraria species complex, which enter a deep diapause and are highly cold-hardy, accumulate larger quantities of triacylglycerols than warm-temperate species, such as D. rufa and D. lutescens, which enter a weak diapause and are less cold-hardy. Among the cool-temperate spcies, D. subauraria occurs at a higher latitude and has the greatest capacity for accumulating triacylglycerols. A subtropical species, D. takahashii, which has no diapause in nature and is not cold-hardy, is unable to store the same quantities of triacylglycerols as temperate species.     

The influence of eclosion timing on winter survival and triacylglycerol accumulation in four temperate species of Drosophila

Abstract. Diapause incidence, winter survival and triacylglycerol content were studied in temperate species of Drosophila by outdoor rearing in Sapporo (a cool-temperate region), northern Japan. In strains of D.subauraria and D.triauraria (cool-temperate species) from northern Japan, diapause was induced in adults having eclosed after early September, but in those having eclosed after mid October in strains of D.rufa and D.lutescens (warm-temperate species) from southern Japan. A subtropical strain of D.triauraria did not enter diapause. In the strains of cool-temperate species from northern Japan, about 70% survived until spring when eclosed in mid autumn, whereas when eclosed earlier and later flies had a lower ability to overwinter. The warm-temperate species and a subtropical strain of D.triauraria also survived longer when eclosed in mid autumn than when eclosed later, but they were unable to survive until spring. The triacylglycerol content was higher in the cool-temperate species from northern Japan than in the warm-temperate species and a subtropical strain of D.trauraria. In each species the triacylglycerol content of adults was higher when they eclosed in early and mid than in late autumn. It is assumed that triacylglycerol plays an important role in overwintering of these Drosophila species and the low triacylglycerol level is the primary cause of the low overwintering capacity of individuals eclosing in late autumn.     

Cold and heat tolerance of drosophilid flies with reference to their latitudinal distributions

The relation between thermal tolerance and latitudinal distribution was studied with 30 drosophilid species collected from the cool-temperate region (Sapporo), the warm-temperate region (Tokyo and Kyoto) and the subtropical region (Iriomote island) in Japan. In addition, intraspecific variation was examined for five species collected from two localities. The subtropical strains of Scaptodrosophila coracina, Drosophila bizonata and D. daruma were less tolerant to cold than their temperate strains. However, the difference of cold tolerance between these two geographic strains was much smaller than the difference between the species restricted to the subtropical region and those occurring in the temperate region. In D. auraria and D. suzukii, no difference was observed in thermal tolerance between their cool- and warm-temperate strains. Thus, geographic variation in thermal tolerance within species was low or negligible. Interspecific comparisons by phylogenetic independent contrasts revealed that species which had the northern boundaries of their distributions at higher latitudes were generally more tolerant to cold than those which had their boundaries at lower latitudes. However, the data for some species did not agree with this trend. The use of man-protected warm places for overwintering, competition or predation would also affect their distributions. It also appeared that species which had their southern boundaries at higher latitudes were generally more cold-tolerant. The acquisition of cold tolerance may lower a flys capacity to compete, survive or reproduce in warmer climates. On the other hand, no relation was observed between heat tolerance and latitudinal distribution. Heat tolerance was higher in species inhabiting openlands or the forest canopy than in those inhabiting the forest understorey.     

Phylogenetic relationships and climatic adaptations in the Drosophila takahashii and montium species subgroups

We analyze phylogenetic relationships among temperate, subtropical highland, and subtropical lowland species of the Drosophila takahashii and montium species subgroups based on sequence data of COI and Gpdh genes and discuss the evolution of temperate species in these subgroups with reference to their climatic adaptations. In the takahashii subgroup, D. lutescens (the temperate species) branched off first in the tree based on the combined data set, but D. prostipennis (the subtropical highland species) branched off first in the trees based on single genes. Thus, phylogenetic relationships in this subgroup are still ambiguous. In the montium subgroup, the cool-temperate species are phylogenetically close to the warm-temperate species, and these cool- and warm-temperate species form a cluster with the subtropical highland species. This suggests that perhaps the cool-temperate species derived from the warm-temperate species and the warm-temperate species derived from the subtropical highland species. In comparison with the subtropical lowland species, the subtropical highland species may be better able to colonize temperate areas since, as in the temperate species, they have an ability to develop their ovaries at moderately low temperature. However, the subtropical highland species, as well as the subtropical lowland species, were much less cold tolerant than the temperate species. Therefore, considerable genetic reformation would be required for both the subtropical highland and the subtropical lowland species to adapt to temperate climates.     

Fish communities in temporarily open/closed estuaries from the warm- and cool-temperate regions of South Africa: A review

The majority of estuaries along the coastline of southern Africa are termed temporarily open/closed estuaries (TOCEs) and are closed off from the sea for varying periods by a sandbar which forms at the mouth. It is therefore important to understand the processes occurring within TOCEs and their importance to fishes in order to make sound management recommendations. Estuaries along the coast of South Africa and their associated fish assemblages are biogeographically distinct and occur in either a subtropical, warm-temperate or cool-temperate zone. There are 125 TOCEs found within the cool-temperate and warm-temperate zones. Most fish species found in TOCEs are the juveniles of marine taxa that breed at sea. Permanently open estuaries generally have a higher diversity of species than TOCEs, but TOCEs still provide important nursery areas for many marine species and numerically often have a higher proportion of estuarine resident species. Important taxa in terms of abundance and biomass in warm-temperate TOCEs include the sparids Rhabdosargus holubi and Lithognathus lithognathus, several mugilid species, estuarine residents (particularly Gilchristella aestuaria and Atherina breviceps) and the freshwater cichlid Oreochromis mossambicus. The diversity of fishes in cool-temperate TOCEs is low when compared with warm-temperate systems and Liza richardsonii tends to dominate catches by number and mass in most systems. Several species recorded in TOCEs show clear longitudinal distribution trends. For example Atherina breviceps is generally more abundant in the lower reaches of estuaries. Mouth state, particularly the frequency, timing and duration of mouth opening plays a key role in determining species richness, composition, diversity and abundance in TOCEs. Mouth state is directly linked to freshwater input. Reduced river inflow leads to prolonged mouth closure and shorter open phases, which inhibits immigration and emigration of marine fish species between estuaries and the sea. Understanding of the effects of various processes occurring within these systems, particularly variation in freshwater input, on the biota of these important systems facilitates the development of informed management recommendations.     

Clinal variation in post‐winter male fertility retention; an adaptive overwintering strategy in Drosophila melanogaster

In insects including Drosophila melanogaster, females can overwinter at the adult stage by adopting a shallow reproductive diapause, but almost nothing is known about male reproductive diapause. In this study, we test for the maintenance of fertility in overwintering males from the eastern Australian D. melanogaster cline. Males from southern temperate populations maintained in field cages in temperate Melbourne had a higher fertility in spring compared with males from tropical locations. Temperate males successfully inseminated more females, and there were also more offspring produced per inseminated female. The resulting linear post‐winter fertility clines were unrelated to male body size. In contrast, there was no clinal variation for fertility in nonoverwintering males held in the laboratory. The cline in overwintering male fertility is likely to have evolved as an adaptive response to latitudinal climatic variation over the last 100 years.     

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.     

Variation in diapause and sex ratio in the parasitoidAsobara tabida

Asobara tabida Nees (Hymenoptera: Braconidae) is a widespread parasitoid, attacking larvae ofDrosophila (Diptera: Drosophilidae) species in fermenting substrates. In this species, geographic variation is found in the percentage of parasitoids entering diapause and in the sex ratio of emerging parasitoids. Percentage diapause appears to be influenced by host species (more parasitoids enter diapause inD. melanogaster Meigen than inD. subobscura Collin) and temperature. It is not correlated with any of the abiotic factors investigated, but is correlated with survival probability inD. melanogaster larvae and with the time of year in which the experiment was conducted (even though none of the parasitoids experienced natural day light). Sex ratio was only found to correlate with percentage diapause, suggesting that males enter diapause more frequently than females. It is concluded thatA. tabida uses diapause to survive both unfavourable abiotic and biotic circumstances.     

How does Drosophila melanogaster overwinter?

In temperate regions low temperatures seem to be the most restrictive factor for survival of Drosophila natural populations, which depends on the capacity of one or more developmental stages to resist unfavourable winter conditions. In this study we have attempted to answer the question of how D. melanogaster overwinters under natural temperature conditions. Only adults overwintered and no diapause was observed in any developmental stage. Thus, developmental duration becomes a decisive component with respect to overwintering potential and, therefore, the preadult stages are unlikely to overwinter. Possible evolutionary steps in adaptation to cold regions are discussed.     

Absence of clinal variation in virgin retention capacity in Australian Drosophila melanogaster

The ability of virgin Drosophila melanogaster adults to retain eggs is thought to be an adaptation to persisting in temperate areas, based on differences in this trait between European and African populations, and based on seasonal changes in this trait in France. By retaining eggs in the absence of males and under conditions of poorer nutrition (conditions common in temperate areas during colder months), females reduce the wastage of resources and increase their probability of surviving spring into summer, enabling them to initiate summer population expansions. To test for variation in virgin egg retention along a climatic gradient, we characterized clinal variation in strains collected from eastern Australia extending from temperate Tasmania to tropical northern Queensland. Despite testing a large number of strains and repeated testing of the cline ends, we did not detect any evidence for clinal variation in virgin egg retention. Therefore although D. melanogaster in temperate Australia overwinter at the adult stage, there is no evidence for selection on virgin retention capacity producing clinal patterns. This contrasts with other evidence for clinal variation in egg production patterns over winter.     

Fruit color and fruit size of bird-disseminated plants in Japan

Fruit color, fruit size and phenology of bird-disseminated plants were examined in different climatic zones of Japan and the relationships between the plants and frugivorous birds were disscussed.Black fruit was the most common in warm-temperate areas and red was the most common in cool-temperate and subarctic zones. Red was more dominant in the lower layer of the forests in all climatic zones. Bicolor fruits were frequent in trees and were not found in herbs. Both in warm- and cool-temperate zones conspicuous fruits which are red and bicolored display were more frequent in summer than in winter.The diameter of most fruits were 4–11 mm. Fruits in warm-temperate were somewhat bigger than those in cooltemperate zone. In forest strata the fruits of shrubs were smaller than those of trees and herbs in width. However I found no relationships between fruit size and fruit color.The frugivorous birds could have influenced not only the evolution of seasonal differences in the proportion of fruit color between warm-temperate and cool-temperate region, but also affect the fruit size.     

Winter sites and cold-hardiness of two gastropod species in a boreal river

Summary The overwintering sites and cold-hardiness of Gyraulus acronicus and Valvata piscinalis were investigated in a northern Swedish river subject to wide seasonal fluctuations in water-level and ice-cover. More than 95% of the population of young and older G. acronicus overwintered in the frozen hydrolittoral zone. No specimens of V. piscinalis were found in the frozen zone. The cold-hardiness in G. acronicus in unfrozen sites was maximal in November and early December. V. piscinalis was not cold-hardy at any time of the year. These interspecific differences in cold-hardiness accord with the differences in overwintering habitats.     

Patterns of transposable element variation and clinality in Drosophila

Natural populations often exist in spatially diverse environments and may experience variation in the strength and targets of natural selection across their ranges. Drosophila provides an excellent opportunity to study the effects of spatially varying selection in natural populations, as both Drosophila melanogaster and Drosophila simulans live across a wide range of environments in North America. Here, we characterize patterns of variation in transposable elements (TEs) from six populations of D. melanogaster and nine populations of D. simulans sampled from multiple latitudes across North America. We find a nearly twofold excess of TEs in D. melanogaster relative to D. simulans, with this difference largely driven by TEs segregating at the lowest and highest allele frequencies. We find no effect of latitude on either total TE abundance or average TE allele frequencies in either species. Moreover, we show that, as a class of mutations, the most common patterns of TE variation do not coincide with the sampled latitudinal gradient, nor are they consistent with local adaptation acting on environmental differences found in the most extreme latitudes. We also do not find a cline in ancestry for North American D. melanogaster—for either TEs or single nucleotide polymorphisms—suggesting a limited role for demography in shaping patterns of TE variation. Though we find little evidence for widespread clinality among TEs in Drosophila, this does not necessarily imply a limited role for TEs in adaptation. We discuss the need for improved models of adaptation to large‐scale environmental heterogeneity, and how these might be applied to TEs.     

Genomic Patterns of Geographic Differentiation in Drosophila simulans

Geographic patterns of genetic differentiation have long been used to understand population history and to learn about the biological mechanisms of adaptation. Here we present an examination of genomic patterns of differentiation between northern and southern populations of Australian and North American Drosophila simulans, with an emphasis on characterizing signals of parallel differentiation. We report on the genomic scale of differentiation and functional enrichment of outlier SNPs. While, overall, signals of shared differentiation are modest, we find the strongest support for parallel differentiation in genomic regions that are associated with regulation. Comparisons to Drosophila melanogaster yield potential candidate genes involved in local adaptation in both species, providing insight into common selective pressures and responses. In contrast to D. melanogaster, in D. simulans we observe patterns of variation that are inconsistent with a model of temperate adaptation out of a tropical ancestral range, highlighting potential differences in demographic and colonization histories of this cosmopolitan species pair.     

Secondary contact and local adaptation contribute to genome‐wide patterns of clinal variation in Drosophila melanogaster

Populations arrayed along broad latitudinal gradients often show patterns of clinal variation in phenotype and genotype. Such population differentiation can be generated and maintained by both historical demographic events and local adaptation. These evolutionary forces are not mutually exclusive and can in some cases produce nearly identical patterns of genetic differentiation among populations. Here, we investigate the evolutionary forces that generated and maintain clinal variation genome‐wide among populations of Drosophila melanogaster sampled in North America and Australia. We contrast patterns of clinal variation in these continents with patterns of differentiation among ancestral European and African populations. Using established and novel methods we derive here, we show that recently derived North America and Australia populations were likely founded by both European and African lineages and that this hybridization event likely contributed to genome‐wide patterns of parallel clinal variation between continents. The pervasive effects of admixture mean that differentiation at only several hundred loci can be attributed to the operation of spatially varying selection using an F_ST outlier approach. Our results provide novel insight into the well‐studied system of clinal differentiation in D. melanogaster and provide a context for future studies seeking to identify loci contributing to local adaptation in a wide variety of organisms, including other invasive species as well as temperate endemics.     

Diapause and cold tolerance in Asian species of the parasitoid Leptopilina (Hymenoptera: Figitidae)

Diapause and cold tolerance are essential for temperate insects to pass the winter, with the mechanisms controlling these two traits varying considerably among insects. In the present study, diapause and cold tolerance are compared among three Leptopilina species: Leptopilina japonica Novkovi? & Kimura, Leptopilina victoriae Nordlander and Leptopilina ryukyuensis Novkovi? & Kimura, all larval parasitoids of frugivorous drosophilid flies, with the aim of understanding their climatic adaptations. The first species is divided into the temperate (Leptopilina japonica japonica) and subtropical subspecies (Leptopilina japonica formosana), and the latter two species are distributed in the tropical and subtropical regions. The temperate subspecies of L. japonica enters prepupal diapause at low temperatures (15 or 18 °C), irrespective of photoperiod, and some individuals enter diapause when exposed to 0 °C for 1 or 2 day(s) or when placed at low humidity. Leptopilina victoriae also shows signs of diapause initiation at 15 °C, although L. ryukyuensis and L. j. formosana from the subtropical regions do not. Preimaginal viability at low temperature (13, 14 or 15 °C) is usually lower in L. victoriae from the tropical regions compared with L. japonica or L. ryukyuensis from the temperate or subtropical regions. Diapausing prepupae of the temperate subspecies appear to be cold tolerant. However, the cold tolerance of nondiapausing prepupae, pupae and adult females varies little among the tropical, subtropical and temperate species or subspecies, and adult males of the temperate subspecies of L. japonica are less cold tolerant than those of the tropical or subtropical species or subspecies. Cold tolerance may be unnecessary, except for diapausing individuals of the temperate species, because nondiapausing individuals appear in warmer seasons.     

Divergence of reaction norms of size characters between tropical and temperate populations of Drosophila melanogaster and D. simulans

Reaction norms to growth temperature of two size-related traits, wing and thorax length, were compared in tropical (West Indies) and temperate (France) populations of the two sibling species, Drosophila melanogaster and D. simulans. A major body size difference was found in D. melanogaster, with much smaller Caribbean flies, while D. simulans exhibited little size variation between geographical populations. The concave norms of reaction were adjusted to second- or third-degree polynomials, and characteristic points calculated i.e. maximum value (MV) and temperature of maximum value (TMV). TMVs were confirmed to be higher for thorax than for wing length, higher in D. melanogaster than in D. simulans, and higher in females than in males. For both traits Caribbean populations exhibited higher TMVs in the two species, strongly suggesting an adaptive shift of the reaction norms toward higher temperature in warm-adapted populations. The wing/thorax ratio was also analysed, and found to be significantly lower in tropical populations of both species. This ratio, which is related to wing loading and flight capacity, might evolve independently of body weight itself.     

Seasonal variation in life history traits in two Drosophila species

Seasonal environmental heterogeneity is cyclic, persistent and geographically widespread. In species that reproduce multiple times annually, environmental changes across seasonal time may create different selection regimes that may shape the population ecology and life history adaptation in these species. Here, we investigate how two closely related species of Drosophila in a temperate orchard respond to environmental changes across seasonal time. Natural populations of Drosophila melanogaster and Drosophila simulans were sampled at four timepoints from June through November to assess seasonal change in fundamental aspects of population dynamics as well as life history traits. D. melanogaster exhibit pronounced change across seasonal time: early in the season, the population is inferred to be uniformly young and potentially represents the early generation following overwintering survivorship. D. melanogaster isofemale lines derived from the early population and reared in a common garden are characterized by high tolerance to a variety of stressors as well as a fast rate of development in the laboratory environment that declines across seasonal time. In contrast, wild D. simulans populations were inferred to be consistently heterogeneous in age distribution across seasonal collections; only starvation tolerance changed predictably over seasonal time in a parallel manner as in D. melanogaster. These results suggest fundamental differences in population and evolutionary dynamics between these two taxa associated with seasonal heterogeneity in environmental parameters and associated selection pressures.     

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.     

Spatially varying selection shapes life history clines among populations of Drosophila melanogaster from sub‐Saharan Africa

Clines in life history traits, presumably driven by spatially varying selection, are widespread. Major latitudinal clines have been observed, for example, in Drosophila melanogaster, an ancestrally tropical insect from Africa that has colonized temperate habitats on multiple continents. Yet, how geographic factors other than latitude, such as altitude or longitude, affect life history in this species remains poorly understood. Moreover, most previous work has been performed on derived European, American and Australian populations, but whether life history also varies predictably with geography in the ancestral Afro‐tropical range has not been investigated systematically. Here, we have examined life history variation among populations of D. melanogaster from sub‐Saharan Africa. Viability and reproductive diapause did not vary with geography, but body size increased with altitude, latitude and longitude. Early fecundity covaried positively with altitude and latitude, whereas lifespan showed the opposite trend. Examination of genetic variance–covariance matrices revealed geographic differentiation also in trade‐off structure, and Q_ST‐F_ST analysis showed that life history differentiation among populations is likely shaped by selection. Together, our results suggest that geographic and/or climatic factors drive adaptive phenotypic differentiation among ancestral African populations and confirm the widely held notion that latitude and altitude represent parallel gradients.