The influence of gene flow on latitudinal clines of photoperiodic adult diapause in the Drosophila auraria species-complex

Temperate species belonging to the Drosophila auraria species complex, D. auraria Peng, D. biauraria Bock & Wheeler, D. triauraria Bock & Wheeler and D. subauraria Kimura, enter reproductive diapause to pass the winter in response to short daylengths. These species from Japan showed latitudinal clines in critical daylength which is longer in populations from higher latitudes. The slopes of these clines coincided well with that of the cline which is approximately predicted from climatic data, suggesting that these clines result from adaptation of the species to the latitudinal gradient of climatic conditions. Between the mainlands and the surrounding islands of Japan, the slopes of clines did not differ significantly, but the deviation from the regression line was usually smaller in mainland populations. It is assumed that gene flow reduces the genetic variation among mainland populations and results in the development of smooth clines. In the plain of east China, D. triauraria did not show clinal variation in critical daylength, although the development of the cline is expected from climatic data. Extensive gene flow among Chinese populations is considered to prevent the development of a cline.     

Geographical variation in photoperiodic induction of larval diapause in the bruchid beetle, Bruchidius dorsalis: polymorphism in overwintering stages

The bruchid beetle, Bruchidius dorsalis Fahraeus (Coleoptera: Bruchidae), has a multivoltine life cycle and shows geographical variation of overwintering stages in Japan. Our previous study found that B. dorsalis enters larval diapause in the final instar under short photoperiods. In cooler areas, we observed that most individuals overwinter in the final larval stage in diapause, whereas beetles at different developmental stages (non‐diapausing young instars, diapausing instars, and adults) were overwintering in warmer areas. In this study, we investigated geographical variation in the photoperiodic response for induction of larval diapause at 20 °C (three populations) and 24 °C (two populations) to clarify the overwintering strategy of B. dorsalis. We observed that (1) diapause incidence at 20 °C changed sharply from ca. 100% to 0% with a change in photoperiod in all the populations, (2) critical photoperiod was longer at 20 °C in populations from cooler areas, and (3) critical photoperiod at 24 °C was shorter than at 20 °C and a fraction of the larvae did not enter diapause, even under short photoperiods. Overwintering stages estimated from these results were consistent with those actually observed in the field. This study indicates that the geographical variation of overwintering stages is likely to reflect adaptive diapause induction in each local environment.     

Parallel Geographic Variation in Drosophila melanogaster

Drosophila melanogaster, an ancestrally African species, has recently spread throughout the world, associated with human activity. The species has served as the focus of many studies investigating local adaptation relating to latitudinal variation in non-African populations, especially those from the United States and Australia. These studies have documented the existence of shared, genetically determined phenotypic clines for several life history and morphological traits. However, there are no studies designed to formally address the degree of shared latitudinal differentiation at the genomic level. Here we present our comparative analysis of such differentiation. Not surprisingly, we find evidence of substantial, shared selection responses on the two continents, probably resulting from selection on standing ancestral variation. The polymorphic inversion In(3R)P has an important effect on this pattern, but considerable parallelism is also observed across the genome in regions not associated with inversion polymorphism. Interestingly, parallel latitudinal differentiation is observed even for variants that are not particularly strongly differentiated, which suggests that very large numbers of polymorphisms are targets of spatially varying selection in this species.     

Geographic variation in diapause induction and mode of diapause inheritance in Tetranychus pueraricola

Abstract:  Diapause induction and photoperiodic response curves were determined for 33 strains of Tetranychus pueraricola derived from kudzu vine at three constant temperatures (15, 18 and 20°C) under a short-day condition (10 : 14 h; light : dark). Females of all but one of the strains entered diapause at all three temperatures with little variation in diapause percentages among the strains. The exception was the southernmost strain, which was found to be a non-diapause (ND) strain. The critical photoperiod gradually decreased towards the south at a rate of about 1 h for each 5 degrees of latitude. The diapause strains (D1 and D2) exhibited 100% diapause, whereas the ND strain exhibited 0% diapause. By crossing these strains, we determined that 'non-diapause' was a dominant character over 'diapause' and the character was controlled by simple Mendelian inheritance. To clarify why the female progeny from the crosses between the D1 and ND strains did not segregate into the diapause and non-diapause phenotypes in a 1:1 ratio in the B₁ generation, round-robin crosses were carried out among the three strains. The results showed that the F₁ generation was reproductively compatible and showed high egg hatchability with a female-biased sex ratio. In the B₁ generation, the crosses between the D1 and ND strains and between the D1 and D2 strains exhibited extremely low egg hatchability and produced mostly female progeny, whereas offspring from the crosses between the D2 and ND strains showed more than 50% hatchability for B₁ eggs and a female-biased sex ratio. Thus, the absence of segregation observed in the crosses between the D1 and ND strains appears to be due to the severe hybrid breakdown that occurred in the B₁ generation.     

Adaptation to a seasonally varying environment: a strong latitudinal cline in reproductive diapause combined with high gene flow in Drosophila montana

Adaptation to seasonal changes in the northern hemisphere includes an ability to predict the forthcoming cold season from gradual changes in environmental cues early enough to prepare for the harsh winter conditions. The magnitude and speed of changes in these cues vary between the latitudes, which induces strong selection pressures for local adaptation.We studied adaptation to seasonal changes in Drosophila montana, a northern maltfly, by defining the photoperiodic conditions leading to adult reproductive diapause along a latitudinal cline in Finland and by measuring genetic differentiation and the amount of gene flow between the sampling sites with microsatellites. Our data revealed a clear correlation between the latitude and the critical day length (CDL), in which half of the females of different cline populations enter photoperiodic reproductive diapause. There was no sign of limited gene flow between the cline populations, even though these populations showed isolation by distance. Our results show that local adaptation may occur even in the presence of high gene flow, when selection for locally adaptive life-history traits is strong. A wide range of variation in the CDLs of the fly strains within and between the cline populations may be partly due to gene flow and partly due to the opposing selection pressures for fly reproduction and overwinter survival. This variation in the timing of diapause will enhance populations' survival over the years that differ in the severity of the winter and in the length of the warm period and may also help them respond to long-term changes in environmental conditions.     

A genetic analysis of photoperiodic reproductive diapause in Drosophila triauraria

Abstract. Recombinant inbred lines were produced from hybrids between diapausing and non-diapausing strains of Drosophila triauraria Bock & Wheeler by twenty generations of full-sib mating. The analysis of these inbred lines suggests that the difference in the photoperiodic response between the original diapausing and non-diapausing strains is due to genes at three or four loci and at least one of these loci is located on the X chromosome. The original diapausing strain and two inbred lines exhibited circadian peaks when subjected to the Nanda-Hamner protocol, although they had different critical daylengths. This suggests that critical daylength is modified independently of the circadian oscillation system in this species. On the other hand, diapause duration was correlated with critical daylength among the inbred lines and the original diapausing strain, suggesting that these two traits are under the control of the same genetic system.     

Geographic variation in photoperiodic diapause induction and diapause intensity in Sericinus montelus (Lepidoptera: Papilionidae)

Abstract Due to the risk of extinction and ornamental value of the swallowtail butterfly, Sericinus montelus Gray (Lepidoptera: Papilionidae) in China, knowledge about local adaptations is important for the conservation and economical utilization of the species. In the present study, photoperiodic diapause induction and diapause intensity of S. montelus populations from Jiamusi (46°37′N), Beijing (40°15′N), Zibo (36°48′N), Fangxian (32°36′N), Wuhan (30°33′N) and Huaihua (27°33′N) were characterized at 25°C. Logistic regression analysis revealed a significant population × hours of light interaction, confirming that photoperiodic responses varied among populations. The critical photoperiod was positively correlated with latitude and increased toward the north at a rate of about 1 h for each 6.67 degrees of latitude. Survival analyses indicated that survival time of diapausing pupae before adult eclosion differed significantly among populations at 25°C and 16 : 8 L : D h. The mean duration of pupal diapause was also positively correlated with latitude. Our study reveals geographic variation in the critical photoperiod for diapause induction and in diapause intensity of S. montelus. These results provide useful information for our general understanding about seasonal adaptation in insects and may also be used to predict how geographic populations respond to climate warming.     

Differences in diapause attributes between two clinal forms distinguished by male-to-male aggression in a subsocial spider mite, Schizotetranychus miscanthi Saito

The nest-weaving spider mite Schizotetranychus miscanthi Saito showed a cline in male-to-male aggression intensity with minimum winter temperature. The altered kin structure in spring nests, which might be caused by winter harshness, was hypothesized to be a key factor responsible for the cline in male-to-male aggression. In Japan, we found two forms (high- and low-aggression forms) that showed different clinal trends with similar regression slopes and different intercepts. The former is characteristic of local populations from milder climates, whereas the latter occurs in harsher climates. We hypothesized that the intensity of female diapause, which may determine whether males are produced during late winter, was one of the factors separating these two clinal forms. In the four populations studied, short day length during the developmental period (egg to adult emergence) induced diapause in females. Diapause intensity varied greatly among populations, and particularly between the high-aggression and low-aggression forms. These data, together with data on winter harshness between the localities, led us to believe that female diapause is one of the factors affecting relatedness between interacting males in nests and can explain why the two forms of S.miscanthi have different clinal trends in male aggression in Japan.     

Latitudinal population differentiation in phenology,life history and flower morphology in the perennial herb Lythrum salicaria

Abstract In plants with a wide distribution, phenological characters can be expected to vary clinally along climatic gradients, whereas other characters important for adaptation to local biotic and abiotic factors may vary in a more mosaic fashion. We used common‐garden experiments and controlled crosses to examine population differentiation in phenology, life history and morphology in the perennial herb Lythrum salicaria along a latitudinal transect through Sweden (57°N to 66°N). Northern populations initiated growth and flowering earlier, flowered for a shorter period, were shorter, produced more and larger winter buds, and were older at first reproduction than southern populations. Flower morphology varied significantly among populations, but was, with the exception of calyx length, not significantly related to latitude of origin. Survival in the common garden (at 63°49′N) was positively correlated with latitude of origin and the size and number of winter buds produced in the preceding year. The results suggest that the among‐population differences in phenology and life history have evolved in response to latitudinal variation in length of the growing season. Further studies are required to determine whether population differentiation in flower morphology is maintained by selection.     

Climatic trends and advancing spring flight of butterflies in lowland California

Many studies, largely from cool‐temperate latitudes, have investigated the relationship between the timing of biological events and changes in climatic conditions during the past few decades. Relatively little is known about the response of plants and animals at lower latitudes. Here we show that the average first spring flight of 23 butterfly species in the Central Valley of California has advanced to an earlier date over the past 31 years. Among the species that have appeared significantly earlier, the average shift is 24 days. Climatic conditions (largely winter temperature and precipitation) are found to explain a large part of the variation in changing date of first flight. These results suggest a strong ecological influence of changing climatic conditions on a suite of animals from a mid‐latitude, Mediterranean climate.     

Photoperiod-dependent adult diapause within a geographical cline in the multivoltine bruchid Bruchidius dorsalis

Abstract The bruchid beetle Bruchidius dorsalis Fahraeus (Coleoptera: Bruchidae) has been known to undergo larval diapause during the final instar under short photoperiods ( Kurota & Shimada, 2001 ). This species has a multivoltine life cycle and the overwintering stages show a geographical variation across Japan ( Kurota & Shimada, 2002 ). In cooler areas, overwintering occurs during the final instar, whereas in warmer climates overwintering can occur during several developmental stages: non‐diapausing young instars, diapausing instars, and adults. In this study, we investigated the adult reproductive diapause in three populations from different geographical regions to clarify the role of geographical variation on overwintering strategies. We found that: (1) B. dorsalis entered reproductive diapause in addition to larval diapause under short photoperiods, (2) diapause propensity was higher and the critical photoperiod was longer in populations from cooler regions, and (3) the sensitive photoperiod range was the first 5 days after emergence. Predictions of the overwintering stage, derived from critical photoperiods, were consistent with actual overwintering stages observed in each population. The geographical variation in diapause induction is likely to reflect the adaptive overwintering strategy in each local environment.     

Genetic basis of photoperiodic control of summer and winter diapause in geographic ecotypes of the rice stem maggot, Chlorops oryzae

Chlorops oryzae Matsumura (Diptera: Chloropidae) is bivoltine in northern Japan but trivoltine in the southern part of the country. Larvae of the bivoltine strain (Akita, 39° N) develop without delay under L14:D10 but enter summer diapause in the mature larval stage under L15:D9. In contrast, larvae of the trivoltine strain (Aichi, 35° N) develop quickly under L15:D9 but enter summer diapause under L14:D10. The genetic basis of their different summer-diapause behavior was analyzed by reciprocal crossing between the two ecotypes and backcrossing to the hybrids. Although a polygenic system seems to be involved, there is a single gene on the X-chromosome exerting a major effect on summer diapause. The northern bivoltine ecotype has a longer critical photoperiod for the induction of winter diapause in the first larval stage and remains in diapause longer than the southern trivoltine ecotype. The differences in the critical photoperiod and the winter diapause duration between the two ecotypes seem to be controlled by a polygenic system but again a sex-linked or closely linked gene (or genes) plays a major role. The two geographic ecotypes differ significantly in summer- and winter-diapause traits, both of which are characterized by sex-linked inheritance. Despite this, no apparent sterility or inviability in hybrids between the ecotypes occurs.     

In search of clinal variation in the period and clock timing genes in Australian Drosophila melanogaster populations

Clinal variation for repeat number in the Thr-Gly region of the period circadian timing gene in Drosophila melanogaster was described in Europe and has subsequently been used as evidence of thermal selection on period alleles. To test for clinal variation in this gene along the east coast of Australia, the period polymorphism was scored on flies from multiple samples collected repeatedly over a 5-year interval, along with variation at another circadian rhythm locus, clock. For period, there was no consistent evidence of clinal variation in the 17 and/or 20 repeat alleles, although when average allele length was examined a weak consistent clinal pattern was detected. For clock there was no evidence of clinal variation in the two most common alleles or in average repeat size. These data are inconsistent with the reported patterns in Europe and suggest that clinal variation in timing genes needs to be re-examined in this region.     

Adaptive latitudinal cline of photoperiodic diapause induction in the parasitoid Nasonia vitripennis in Europe

Living in seasonally changing environments requires adaptation to seasonal cycles. Many insects use the change in day length as a reliable cue for upcoming winter and respond to shortened photoperiod through diapause. In this study, we report the clinal variation in photoperiodic diapause induction in populations of the parasitoid wasp Nasonia vitripennis collected along a latitudinal gradient in Europe. In this species, diapause occurs in the larval stage and is maternally induced. Adult Nasonia females were exposed to different photoperiodic cycles and lifetime production of diapausing offspring was scored. Females switched to the production of diapausing offspring after exposure to a threshold number of photoperiodic cycles. A latitudinal cline was found in the proportion of diapausing offspring, the switch point for diapause induction measured as the maternal age at which the female starts to produce diapausing larvae, and the critical photoperiod for diapause induction. Populations at northern latitudes show an earlier switch point, higher proportions of diapausing individuals and longer critical photoperiods. Since the photoperiodic response was measured under the same laboratory conditions, the observed differences between populations most likely reflect genetic differences in sensitivity to photoperiodic cues, resulting from local adaptation to environmental cycles. The observed variability in diapause response combined with the availability of genomic tools for N. vitripennis represent a good opportunity to further investigate the genetic basis of this adaptive trait.     

Latitudinal compensation in female reproductive rate of a geographically widespread reef fish

Latitudinal variation in fitness-related traits has often been attributed to local adaptation to climates. In poikilotherms including fishes, lower temperatures and shorter reproductive seasons at high latitudes would be expected to cause a reduction in annual reproductive output of an individual. Theories of latitudinal compensation predict that organisms at high latitudes should evolve compensatory responses for these climatic effects. Therefore, latitudinal compensation in female reproductive rate (egg production rate), that individuals from high latitudes produce eggs at higher rates than those from lower latitudes, is likely to occur. I tested this hypothesis with a latitudinally widespread reef fish Pomacentrus coelestis that is a multiple batch spawner, from three different localities, from temperate to subtropical waters, within Japan. I used common-environment experiments at three different temperatures to compare reproductive capacity among local populations. In the experiments, average inter-spawning intervals were the shortest and average size-specific clutch weight was the heaviest in fish from the most northern locality across all temperatures, showing clear latitudinal clines. Thus, the northern fish can achieve higher reproductive output per unit time both by shortening inter-spawning intervals and increasing size-specific clutch weight. Additionally, faster egg production rate of the northern fish did not result from increased food consumption. This finding suggests that gross egg production efficiency was higher in the northern fish and that northern fish had a superior capacity for reproduction within a season. These results support the prediction that latitudinal compensation occurs in the female reproductive rate of P. coelestis. As the reproductive season of this species decreases drastically with increasing latitude, the observed cline in the reproductive rate must be an adaptive response to the local selective regime, i.e., length of the reproductive season. Such latitudinal compensation in female reproductive rates may be a common pattern in latitudinally widespread fishes.     

Effects of photoperiodically induced reproductive diapause and cold hardening on the cold tolerance of Drosophila montana

Coping with seasonal and daily variation in environmental conditions requires that organisms are able to adjust their reproduction and stress tolerance according to environmental conditions. Females of Drosophila montana populations have adapted to survive over the dark and cold winters at high latitudes and altitudes by spending this season in photoperiodically controlled reproductive diapause and reproducing only in spring/summer. The present study showed that flies of a northern population of this species are quite tolerant of low temperatures and show high seasonal and short-term plasticity in this trait. Culturing the flies in short day length (nearly all females in reproductive diapause), as well as allowing the flies to get cold hardened before the cold treatment, increased the cold tolerance of both sexes both in chill coma recovery time test and in mortality assay. Chill coma recovery time test performed for the females of two additional D. montana populations cultured in a day length where about half of the females enter diapause, also showed that diapause can increase female cold tolerance even without a change in day length. Direct linkage between diapause and cold tolerance was found in only two strains representing a high-altitude population of the species, but the phenomenon will certainly be worth of studying in northern and southern populations of the species with larger data sets.     

Timing of photoperiodic competency causes phenological mismatch in balsam poplar (Populus balsamifera L.)

Plant phenology is expected to be sensitive to climate warming. In boreal trees, spring flush is primarily temperature driven, whereas height growth cessation and autumn leaf senescence are predominantly controlled by photoperiod. Cuttings of 525 genotypes from the full range of balsam poplar were planted into two common gardens (Vancouver and Indian Head, Canada) at similar latitudes, but with differing winter temperatures and growing seasons. There was clinal variation in spring and, particularly, summer and fall phenology. Bud flush and, despite milder climate, bud set and leaf drop were earlier at Vancouver than at Indian Head by 44, 28 and 7 d, respectively. Although newly flushed growth is insensitive to photoperiod, many genotypes at both sites became competent before the summer solstice. At Vancouver, high‐latitude genotypes set dormant terminal buds in mid‐spring. Most other genotypes grew until midsummer or set bud temporarily and then experienced a second flush. In both gardens and in a growth chamber experiment, earlier bud set was associated with reduced height growth and higher root/shoot ratios. Shoots attained competency ～5 weeks after flushing, which would normally prevent dormancy induction before the solstice, but may be insufficient if spring advances by more than a few weeks.     

The role of latitudinal,genetic and temperature variation in the induction of diapause of Papilio glaucus (Lepidoptera: Papilionidae)

A key adaptation in insects for dealing with variable environmental conditions is the ability to diapause. The tiger swallowtail butterflies, Papilio glaucus and P. canadensis are ideal species to explore the genetic causes and population genetic consequences of diapause because divergence in this trait is believed to be a salient factor in maintaining a hybrid zone between these species. Yet little is known about the factors that influence diapause induction in this system. Here we explored how spatial (latitudinal), environmental (temperature) and genetic (hybridization) factors affect diapause induction in this system. Specifically, a series of growth chamber experiments using wild caught individuals from across the eastern United States were performed to: (1) evaluate how critical photoperiod varies with latitude, (2) isolate the stage in which induction occurs, (3) test whether changes in temperature affected rates of diapause induction, and (4) explore how the incidence of diapause is affected in hybrid offspring. We find that induction occurs in the larval stage, is not sensitive to a relatively broad range of temperatures, appears to have a complex genetic basis (i.e., is not simply a dominant trait following a Mendelian inheritance pattern) and that the critical photoperiod increases by 0.4 h with each increasing degree in latitude. This work deepens our understanding of how spatial, environmental and genetic variation influences a key seasonal adaptation (diapause induction) in a well‐developed ecological model system and will make possible future studies that explore how climatic variation affects the population dynamics and genetics of this system.     

Aestivo-hibernal reproductive diapause in Drosophila moriwakii: flight as a controlling factor

Drosophila moriwakii Okada & Kurokawa (Diptera; Drosophilidae) generally has only one generation per year and enters aestivo-hibernal reproductive diapause in Sapporo, northern Japan, but a small fraction of the population produced a second generation in summer at a place where breeding resources were abundant. In this species, diapause seems to be controlled by flight activity. When flies were cultured in cages in which they were able to fly freely, they entered diapause irrespective of photoperiod, but they did not do so at long daylengths when cultured in small vials in which they were prevented from flying. Furthermore, flies with wings removed did not enter diapause at long daylengths even if they were cultured in the cages.     

Temperature‐correlated shifts in the timing of egg‐laying in House Finches Haemorhous mexicanus

Although temperature‐correlated shifts in the timing of egg‐laying have been documented in numerous bird species, the vast majority of species examined to date have been those that breed in Europe and have an animal‐based diet during breeding. However, given that the timing of breeding can be driven, either in the proximate or in the ultimate sense, by seasonal fluctuations in food availability, the relationship between temperature and laying may differ with diet. Here, we report on patterns of reproductive timing in House Finches Haemorhous mexicanus, a North American species that breeds on a primarily seed‐based diet. Analysing nest records from House Finches in California spanning more than a century, we found that egg‐laying occurred significantly earlier in warmer springs. We also found that although the timing of egg‐laying does not show long‐term changes in most of California, in the hottest region of the state (the southeast desert basin) it has advanced significantly.