* Your assessment is very important for improving the workof artificial intelligence, which forms the content of this project
Download Dominant and Recessive Inheritance Patterns of
Survey
Document related concepts
Hybrid (biology) wikipedia , lookup
Pharmacogenomics wikipedia , lookup
Inbreeding avoidance wikipedia , lookup
Genome (book) wikipedia , lookup
Public health genomics wikipedia , lookup
Polymorphism (biology) wikipedia , lookup
Genetic drift wikipedia , lookup
Medical genetics wikipedia , lookup
Heritability of IQ wikipedia , lookup
Behavioural genetics wikipedia , lookup
Koinophilia wikipedia , lookup
Population genetics wikipedia , lookup
Human genetic variation wikipedia , lookup
Pathogenomics wikipedia , lookup
Microevolution wikipedia , lookup
Transcript
Journal of Heredity 2010:101(1):20–25 doi:10.1093/jhered/esp085 Advance Access publication October 21, 2009 Ó The American Genetic Association. 2009. All rights reserved. For permissions, please email: [email protected]. Dominant and Recessive Inheritance Patterns of Diapause in the Two-Spotted Spider Mite Tetranychus urticae YUKO KAWAKAMI, HIDEHARU NUMATA, KATSURA ITO, AND SHIN G. GOTO From the Department of Biology and Geosciences, Graduate School of Science, Osaka City University, Osaka 558-8585, Japan (Kawakami, Numata, and Goto); the JST Innovation Satellite Kochi, Kochi 782-8502, Japan (Ito); and the Laboratory of Applied Entomology, Faculty of Agriculture, Kochi University, Kochi 783-8502, Japan (Ito). Hideharu Numata is now at the Department of Zoology, Graduate School of Science, Kyoto University, Sakyo, Kyoto 606-8502, Japan. Address correspondence to Shin G. Goto at the address above, or e-mail: [email protected]. Abstract In this study, we investigated the diapause incidence in 3 geographic strains of the two-spotted spider mite Tetranychus urticae (Acari: Tetranychidae). Under diapause-inducing conditions of 12:12 light:dark at 15 °C, the diapause incidence was nearly 100% in a strain from northern Japan (Sapporo), whereas it was nearly 0% in 2 strains from southern Japan (Itoman and Takanabe). Reciprocal crosses clearly showed that the nondiapause phenotype is inherited in a completely dominant manner, and no maternal effect was detected. Backcrosses to the Itoman and Takanabe strains suggested that dominant nondiapause alleles control the nondiapause phenotype. To clarify the genetic basis of nondiapause in the northern population, we also established a nondiapausing variant (‘‘selected nondiapause’’ abbreviated as snd) from the Sapporo strain. Crossing experiments revealed that a single recessive allele is responsible for the nondiapause phenotype. Thus, both dominant and recessive inheritance patterns of diapause were detected in the T. urticae populations studied here. Key words: artificial selection, diapause, genetic basis, geographic variation, Tetranychidae Diapause is a form of dormancy in arthropods, which is characterized by developmental arrest; it confers survival advantages during unfavorable seasonal conditions, such as during winter (Denlinger 2002). It is well known that geographic differences exist in the occurrence of diapause in many arthropods (reviewed by Tauber et al. 1986; Saunders 2002). Most populations of species inhabiting temperate regions undergo photoperiodic diapause, but those populations inhabiting tropical regions do not (Danks 1987). For example, a Japanese strain of the flesh fly Sarcophaga peregrina enters pupal diapause in response to short daylength, whereas a certain New Guinean strain of this species does not (Kurahashi and Ohtaki 1977). An Arizonian strain of the pink bollworm Pectinophora gossypiella enters larval diapause, whereas a certain Indian strain of this species does not (Raina and Bell 1974). It is widely accepted that such differences in diapause potential are due to the considerable genetic polymorphism formed by selective forces (Tauber et al. 1986). Genetic studies related to diapause have shown various modes of inheritance in different species (Danks 1987). Some species have been reported to have polygenic systems 20 (e.g., Kurahashi and Ohtaki 1977; Wipking and Kurtz 2000), whereas several studies have revealed that in other species diapause can be determined by only a small subset of ‘‘diapause/nondiapause genes’’ (e.g., Zinovyeva 1980; Henrich and Denlinger 1983; Doležel et al. 2005; Han and Denlinger 2009). The two-spotted spider mite Tetranychus urticae (Acari: Tetranychidae) is known to be a serious pest affecting the agroecosystem and is extensively distributed worldwide. The females of this spider mite overwinter by undergoing adult diapause in response to short daylength and low temperature during their immature development. In contrast, males, which are hemizygous offspring that develop from unfertilized eggs (Helle and Bolland 1967), do not enter diapause. Geographic variation in diapause potential has also been reported in T. urticae: Tetranychus urticae in regions with a mild winter climate do not enter diapause, whereas those inhabiting regions with a cooler climate enter diapause in winter (Gotoh and Shinkaji 1981; Veerman 1985; Takafuji et al. 1991; Koveos et al. 1993). Here, we performed interstrain crosses using 3 geographic strains of T. urticae, in order to elucidate the genetic Kawakami et al. Genetics of Diapause in the Two-Spotted Spider Mite basis of diapause. In the present study, we detected dominant ‘‘nondiapause alleles’’ in southern populations. In addition, we established a variant from a strain with high diapause incidence. This variant does not enter diapause even under strong diapause-inducing conditions. Interstrain crosses between the variant and the original strain clarified that a single recessive nondiapause allele is hidden in the northern population. Materials and Methods Mites Three strains of T. urticae, one from northern Japan (Sapporo) and the other 2 from southern Japan (Itoman and Takanabe), were used in the present study (Table 1). More than 100 individuals were collected in Sapporo. They were reared on detached leaves of the kidney bean Phaseolus vulgaris L., placed on water-soaked cotton in plastic cases (90 70 23 mm), under diapause-averting long-day conditions with a 16:8 light:dark (L:D) photoperiod at 25 °C. The strain was maintained for more than 40 generations in the laboratory under the above mentioned conditions. Similarly, more than 50 individuals from Itoman and more than 50 individuals from Takanabe were collected and maintained for more than 20 and 30 generations, respectively. Hereafter, we will refer to the Sapporo strain as the D strain, the Itoman strain as the ND1 strain, and the Takanabe strain as the ND2 strain. Establishment of a Nondiapausing Variant A variant strain that did not enter diapause even under diapause-inducing conditions was established from the D (Sapporo) strain. When the D strain was reared under diapause-inducing short-day conditions (12:12 L:D at 15 °C), some females averted diapause (see Results). We collected the nondiapausing females and maintained them under the same short-day conditions. Later, they produced male and female progeny, and the progeny mated and laid eggs. We collected the eggs and maintained them under the same short-day conditions. This selection procedure was repeated twice, and the diapause incidence finally reduced to a low value (see Results). We named this strain ‘‘selected nondiapause’’ (snd) variant. Crosses Reciprocal crosses (females shown on the left) between geographic strains were performed as follows: D ND1, ND1 D, D ND2, and ND2 D. Reciprocal crosses Table 1. between the D and snd strains were also performed, that is, D snd and snd D. Twenty female deutonymphs (the second (last) nymphal stage) of each strain were individually transferred onto bean leaves, cut into 10 10 mm squares, and were maintained under 16:8 L:D conditions at 25 °C. During the last quiescent stage, a single adult male of the opposite strain was placed on the leaf for at least 24 h so that the mites could copulate. Adult females were transferred onto a new piece of leaf every day until day 7. The progeny was reared under 12:12 L:D conditions at 15 °C. Backcrosses between F1 females and males of the parental strain were performed as follows: (D ND1) ND1, (ND1 D) ND1, (D ND2) ND2, (ND2 D) ND2, (D snd) D, (snd D) D, (D snd) snd, and (snd D) snd. F1 progeny from reciprocal crosses were maintained under diapause-averting conditions—16:8 L:D at 25 °C—in order to avoid an environmentally induced reduction in diapause incidence due to factors associated with diapause history, such as maternal effect. Twenty female deutonymphs belonging to the F1 progeny were individually transferred onto the bean leaf squares (10 10 mm) and were reared under 16:8 L:D at 25 °C. During the last quiescent stage, a single adult male of the opposite strain was placed on the leaf for at least 24 h so that the mites could copulate. Adult females were transferred onto a new leaf piece every day until day 7. The eggs laid by the females were reared under 12:12 L:D conditions at 15 °C. Backcrosses to D, ND, and snd were described as BC-D, BC-ND, and BC-snd, respectively. The crosses between geographic strains were performed twice, and data from the replicates were combined. Crosses between the D and snd strains were performed once. Determination of Diapause Status After adult emergence, the female progeny were collected daily. On day 6, they were individually transferred onto the bean leaf squares (10 10 mm). Their diapause status was examined by their body color and oviposition status. Kawakami et al. (2009) found that all the females in whom the body color had changed from green to orange by day 12 showed suppressed ovarian development and laid no eggs. Thus, females with orange body color after day 7 were determined to be diapausing individuals, whereas females in whom the body color did not change within 12 days of adult emergence were determined to be nondiapausing individuals. We also found that a small proportion of females with green or intermediate body color laid no eggs. Therefore, they were dissected on day 12 in 0.9% NaCl solution under a stereoscopic microscope (SMZ1500; Nikon, Tokyo, Tetranychus urticae strains used in the present study Strain Collection locality Date of collection Host plant D ND1 ND2 Sapporo, Hokkaido (43.07°N, 141.34°E) Itoman, Okinawa (26.10°N, 127.69°E) Takanabe, Miyazaki (32.11°N, 131.52°E) 7 June 2006 6 July 2007 6 and 7 January 2007 Lamium purpureum Phaseolus vulgaris Rosa hybrida 21 Journal of Heredity 2010:101(1) Japan). Females in whom yolk deposition was observed in the ovary were determined to be nondiapausing individuals, whereas those in whom yolk deposition was not observed were determined to be diapausing individuals, as reported in Kawakami et al. (2009). Results Diapause Incidence in the Geographic Strains Table 2 shows the diapause incidence in geographic strains under 12:12 L:D conditions at 15 °C. The diapause incidence in the D strain from northern Japan was nearly 100%, whereas it was nearly 0% in both the southern strains (ND1 and ND2). located on distinct chromosomes, the ratio of the diapause incidence in the BC-D and that in the parental D will be 1:4. Both backcrosses, (D ND2) D and (ND2 D) D, produced progeny with a diapause incidence of nearly 25%. The values were significantly different from the value expected when a single locus governs the nondiapause phenotype (v2 test, P , 0.05; Figure 1) but were close to the value expected when 2 loci located on distinct chromosomes govern the nondiapause phenotype (v2 test, P . 0.05; Figure 1). The (D ND1) D and (ND1 D) D backcrosses produced progeny with a diapause incidence of Crosses between Geographic Strains The diapause incidence in the F1 progeny produced from the cross between the D and ND strains was nearly 0% under 12:12 L:D at 15 °C, irrespective of the direction of the crosses (Table 2). The results clearly indicate that in both ND strains, the nondiapause phenotype is inherited in a dominant manner; moreover, no maternal effect was detected. The diapause incidence in the progeny produced from backcrosses between F1 females and ND males was nearly 0%, irrespective of the genotype of the female (Table 2). This also indicates that the nondiapause phenotype has a dominant inheritance pattern. When a dominant allele at a single locus governed the nondiapause phenotype, the ratio of the diapause incidence in the BC-D and that in the parental D will be close to 1:2. When the nondiapause phenotype was governed by dominant alleles at 2 loci Table 2. Diapause incidence in parental strains, F1 progeny from reciprocal crosses, and backcross progeny between D and ND strains, under 12:12 L:D at 15 °C in Tetranychus urticae Strain/hybrid %diapause N P D ND1 ND2 94.0 0.3 0.3 430 306 292 0.7 0.2 1.4 0.7 1064 1279 697 1065 43.3 36.3 25.4 25.6 1341 761 1098 399 0.6 0.2 3.6 0.7 1076 2107 393 1099 F1 D ND1 ND1 D D ND2 ND2 D BC-D (D ND1) (ND1 D) (D ND2) (ND2 D) BC-ND (D ND1) (ND1 D) (D ND2) (ND2 D) 22 D D D D ND1 ND1 ND2 ND2 Figure 1. Comparisons of diapause incidence in Tetranychus urticae with theoretically predicted values by a Mendelian inheritance model in 3 crosses: crosses between ND1 and D strains (A), those between ND2 and D strains (B), and those between snd and D strains (C). Backcross with the D, ND, and snd males are shown as BC-D, BC-ND, and BC-snd, respectively. Single: the expected value when a single locus governs the nondiapause phenotype; double: the expected value when 2 loci on distinct chromosomes govern the nondiapause phenotype. (v2 test, *P , 0.05, ns: not significantly different from the expected value at the 5% level). See also Tables 2 and 3. Kawakami et al. Genetics of Diapause in the Two-Spotted Spider Mite 43.3% and 36.3%, respectively; these incidence values were significantly different from the value expected when a single locus governs the nondiapause phenotype and from the value expected when 2 loci on distinct chromosomes govern the nondiapause phenotype (v2 test, P , 0.05; Figure 1). Establishment of a Nondiapausing Variant The snd strain, which did not enter diapause even under diapause-inducing conditions, was established as the nondiapausing variant. We observed a diapause incidence of 96.0% in the parental D (N 5 470). As a result of selection, this incidence decreased to 13.6% (N 5 413). The subsequent selection resulted in a diapause incidence of 2.5% (N 5 529). The rapid drop in diapause incidence, which was observed after selection, suggests that the nondiapause phenotype in this variant is governed by a small number of loci. Crosses between the D Strain and Variant Strain The diapause incidence in the F1 progeny produced from the cross between the D and snd strains was nearly 94% under 12:12 L:D at 15 °C, irrespective of the direction of the crosses (Table 3). The results clearly indicate that nondiapause is inherited in a recessive manner; moreover, no maternal effect was detected. The diapause incidence in the progeny produced from backcrosses between F1 females and D males was higher, irrespective of the genotype of the female (Table 3). This also indicates that the nondiapause phenotype has a recessive inheritance pattern. The backcrosses between F1 females and snd males produced progeny with a diapause incidence of nearly 50%, and the incidences were not significantly different from the value expected if a single loci is involved in the expression of diapause (v2 test, P . 0.05; Figure 1). Discussion The present study revealed that the D strain from northern Japan has a diapause incidence of nearly 100% under 12:12 L:D at 15 °C, whereas the ND1 and ND2 strains from southern Japan exhibit a diapause incidence of nearly 0% under the same conditions. A latitudinal cline in diapause incidence has been reported in many insects inhabiting temperate regions (Danks 1987). Gotoh and Shinkaji (1981) also reported a latitudinal cline in diapause potential in T. urticae. In the present study, it is still uncertain whether the mites of ND1 and ND2 still retain the ability to respond to nonphotoperiodic cues for induction of diapause. The reciprocal crosses and backcrosses conducted here indicate that the nondiapause phenotype found in both the southern populations is completely dominant over the diapause phenotype in the northern population. Such dominant inheritance of the nondiapause phenotype was also reported in some insects, such as the black field cricket Teleogryllus commodus (Hogan 1966) and the redheaded pine sawfly Neodiprion lecontei (Knerer 1983). Table 3. Diapause incidence in D and snd (selected nondiapause) strains, F1 progeny from reciprocal crosses, and backcross progeny between the strains, under 12:12 L:D at 15 °C in Tetranychus urticae Strain/hybrid %diapause N P D snd 96.0 2.5 470 529 95.3 94.4 1228 1131 D D 89.6 94.3 1268 1234 snd snd 46.5 49.6 1104 1127 F1 D snd snd D BC-D (D snd) (snd D) BC-snd (D snd) (snd D) On the basis of the results of both backcrosses, that is, (D ND2) D and (ND2 D) D, we think that dominant alleles at 2 loci on distinct chromosomes control the nondiapause phenotype in the ND2 (Takanabe) strain. In contrast, the diapause incidence in the progeny produced from the backcrosses (D ND1) D and (ND1 D) D was around 40%. These values were significantly different from the values expected when a dominant nondiapause allele at a single locus or dominant nondiapause alleles at 2 loci on distinct chromosomes govern the nondiapause phenotype. Dominant nondiapause alleles at 2 or more loci located on the same chromosome, which were loosely linked, may control the nondiapause phenotype in the ND1 (Itoman) strain. Thus, these major genes found in the ND strains are responsible for the inability of the mites to enter diapause, despite the presence of strong diapause-inducing conditions. In the present study, we established a nondiapausing variant (snd) from the strain with high diapause incidence, in order to elucidate the genetic basis of nondiapausing individuals found in the northern population. Reciprocal crosses and backcrosses indicated that the nondiapause phenotype in the snd was inherited in a recessive manner, and a single locus is responsible for the nondiapause phenotype. Ignatowicz and Helle (1986) and Goka and Takafuji (1990) also reported similar results in a Dutch strain and a Japanese strain of T. urticae, respectively. It has been reported that the variation in diapause potential in T. urticae populations can be attributed to various genetic systems including dominant alleles at multiple loci (as found in the present study), a recessive allele at a single locus (the present study; Ignatowicz and Helle 1986), incompletely recessive alleles at multiple loci (Goka and Takafuji 1990, 1991; So and Takafuji 1992), and a cytoplasmic factor (Goka and Takafuji 1990, 1991). Saunders (2002) proposed a model for photoperiodic diapause that comprised a photoperiodic photoreceptor, a photoperiodic clock, and an output. The clock is subdivided into a photoperiodic time measurement system 23 Journal of Heredity 2010:101(1) and a counter. A circadian clock is clearly involved in the photoperiodic clock (Saunders 2002). Thus, it is plausible that mutations in any of the genes involved in the cascade will have various effects on the induction of diapause. This further indicates that the loci responsible for the diapause/ nondiapause phenotype are not necessarily homologous in various species or even in strains in a single species. Various inheritance patterns of diapause in the T. urticae populations (Ignatowicz and Helle 1986; Goka and Takafuji 1990, 1991; So and Takafuji 1992; the present study) suggest that several different loci are involved in the diapause induction, diapause can be affected by various types of alterations in any one of the loci, and therefore, alterations at different loci can generate various modes of inheritance of diapause (see also Vaz Nunes et al. 1990). Diapause is usually correlated with other traits, and this correlation is helpful for genetically dissecting the physiological mechanisms underlying photoperiodic response as shown in several species, that is, the face fly Musca autumnalis, the drosophilid fly Chymomyza costata, and some flesh fly species of Sarcophaga (Henrich and Denlinger 1983; Kim et al. 1995; Koštál and Shimada 2001; Pavelka et al. 2003; Goto et al. 2006; Goto 2009). However, the ND and snd strains in the present study did not exhibit any noticeable developmental and morphological differences, and therefore, the roles of the detected loci in the photoperiodic induction of diapause are still unclear. Our long-term goals are to identify the loci found in the ND and snd strains and clarify their roles in photoperiodic regulation. Quantitative trait loci (QTLs) analyses have brought to light a single region of the genome that includes loci contributing diapause traits in Drosophila melanogaster in some mosquitoes belonging to the Culex pipiens complex and in Wyeomyia smithii (Mathias et al. 2007; Mori et al. 2007; Schmidt et al. 2008). Linkage analysis is also a powerful tool for verifying the loci governing the nondiapause phenotype (Pavelka et al. 2003). A recent genome project for elucidating the genomic sequences in T. urticae has almost reached completion (http://www.jgi.doe.gov/). This genome information along with QTLs and linkage analyses would greatly contribute to identifying these nondiapause loci in T. urticae. Acknowledgments We thank Dr Yoshinori Shintani, Minami Kyushu University and Dr Takane Sakagami, Hokkai Sankyo Co., Ltd., for collecting the animals. Goka K, Takafuji A. 1990. Genetic studies on the diapause of the twospotted spider mite, Tetranychus urticae Koch (1). Appl Entomol Zool. 25: 119–125. Goka K, Takafuji A. 1991. Genetic studies on the diapause of the twospotted spider mite Tetranychus urticae Koch (2). Appl Entomol Zool. 26:77–84. Goto SG. 2009. Genetic analysis of diapause capability and association between larval and pupal photoperiodic responses in the flesh fly Sarcophaga similis. Physiol Entomol. 34:46–51. Goto SG, Han B, Denlinger DL. 2006. A nondiapausing variant of the flesh fly, Sarcophaga bullata, that shows arrhythmic adult eclosion and elevated expression of two circadian clock genes, period and timeless. J Insect Physiol. 52:1213–1218. Gotoh T, Shinkaji N. 1981. Critical photoperiod and geographical variation of diapause induction in the two-spotted spider mite, Tetranychus urticae Koch (Acarina, Tetranychidae), in Japan. Jpn J Appl Entomol Zool. 25:113–118. (in Japanese with English summary). Han B, Denlinger DL. 2009. Mendelian inheritance of pupal diapause in the flesh fly, Sarcophaga bullata. J Hered. 100:251–255. Helle W, Bolland HR. 1967. Karyotypes and sex-determination in spider mites (Tetranychidae). Genetica. 38:43–53. Henrich VC, Denlinger DL. 1983. Genetic differences in pupal diapause incidence between two selected strains of the flesh fly. J Hered. 74: 371–374. Hogan TW. 1966. Some diapause characteristics and interfertility of three geographic populations of Teleogryllus commodus (Walk.) (Orthoptera: Gryllidae). Aust J Zool. 13:455–459. Ignatowicz S, Helle W. 1986. Genetics of diapause suppression in the two-spotted spider mite, Tetranychus urticae Koch. Exp Appl Acarol. 2: 161–172. Kawakami Y, Goto SG, Ito K, Numata H. 2009. Suppression of ovarian development and vitellogenin gene expression in the adult diapause of the two-spotted spider mite Tetranychus urticae. J Insect Physiol. 55:70–77. Kim Y, Krafsur ES, Bailey TB, Zhao SL. 1995. Mode of inheritance of face fly diapause and its correlation with other developmental traits. Ecol Entomol. 20:359–366. Knerer G. 1983. Diapause strategies in diprionid sawflies. Naturwissenschaften. 70:203–205. Koštál V, Shimada K. 2001. Malfunction of circadian clock in the nonphotoperiodic-diapause mutants of the drosophilid fly, Chymomyza costata. J Insect Physiol. 47:1269–1274. Koveos DS, Kroon A, Veerman A. 1993. Geographic variation of diapause intensity in the spider mite Tetranychus urticae. Physiol Entomol. 18:50–56. Kurahashi H, Ohtaki T. 1977. Crossing between non-diapausing and diapausing races of Sarcophaga peregrina. Experientia. 33:186–187. Mathias D, Jacky L, Bradshaw WE, Holzapfel CM. 2007. Quantitative trait loci associated with photoperiodic response and stage of diapause in the pitcher-plant mosquito, Wyeomyia smithii. Genetics. 176:391–402. References Mori A, Romero-Severson J, Severson DW. 2007. Genetic basis for reproductive diapause is correlated with life history traits within the Culex pipiens complex. Insect Mol Biol. 16:515–524. Danks HV. 1987. Insect dormancy: an ecological perspective. Ottawa (Canada): Biological Survey of Canada. Pavelka J, Shimada K, Koštál V. 2003. TIMELESS: a link between fly’s circadian and photoperiodic clocks? Eur J Entomol. 100:255–265. Denlinger DL. 2002. Regulation of diapause. Annu Rev Entomol. 47:93–122. Raina AK, Bell RA. 1974. Nondiapausing strain of pink bollworm from southern India. Ann Entomol Soc Am. 67:685–686. Doležel D, Vanecková H, Šauman I, Hodkova M. 2005. Is period gene causally involved in the photoperiodic regulation of reproductive diapause in the linden bug, Pyrrhocoris apterus? J Insect Physiol. 51:655–659. Saunders DS. 2002. Insect clocks. Amsterdam (The Netherlands): Elsevier. 24 Schmidt PS, Zhu CT, Das J, Batavia M, Yang L, Eanes WF. 2008. An amino acid polymorphism in the couch potato gene forms the basis for Kawakami et al. Genetics of Diapause in the Two-Spotted Spider Mite climatic adaptation in Drosophila melanogaster. Proc Natl Acad Sci USA. 105:16207–16211. So PM, Takafuji A. 1992. Local variation in diapause characteristics of Tetranychus urticae Koch (Acarina: Tetranychidae). Oecologia. 90:270–275. Takafuji A, So PM, Tsuno N. 1991. Inter-population and intra-population variations in diapause attribute of the two-spotted spider mite, Tetranychus urticae Koch, in Japan. Res Popul Ecol. 33:331–344. Tauber MJ, Tauber CA, Masaki S. 1986. Seasonal adaptations of insects. Oxford (UK): Oxford University Press. Vaz Nunes M, Koveos DS, Veerman A. 1990. Geographical variation in photoperiodic induction of diapause in the spider mite (Tetranychus urticae): a causal relation between critical nightlength and circadian period? J Biol Rhythms. 5:47–57. Veerman A. 1985. Diapause. In: Helle W, Sabelis MW, editors. Spider mites: their biology, natural enemies and control. Vol. 1A. Amsterdam (The Netherlands): Elsevier. p. 279–316. Wipking W, Kurtz J. 2000. Genetic variability in the diapause response of the burnet moth Zygaena trifolii (Lepidoptera: Zygaenidae). J Insect Physiol. 46:127–134. Zinovyeva KB. 1980. Inheritance of larval diapause in the crossing of two geographic forms of Calliphora vicina R.-D. (Diptera, Calliphoridae). Entomol Rev. 59:9–20. Received March 29, 2009; Revised June 30, 2009; Accepted September 3, 2009 Corresponding Editor: Rob DeSalle 25