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Journal of Heredity 2010:101(1):20–25
doi:10.1093/jhered/esp085
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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.
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Received March 29, 2009; Revised June 30, 2009;
Accepted September 3, 2009
Corresponding Editor: Rob DeSalle
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