Appl. Entomol. Zool. 42 (3): 383–389 (2007) http://odokon.org/
Maternal photoperiod effect on and geographic variation of diapause incidence in Cotesia plutellae (Hymenoptera: Braconidae) from China Umsalama A. M. AHMED, Zu-hua SHI,* Yu-ling GUO, Xiang-fei ZOU, Zhong-ping HAO and Shu-ting PANG Institute of Insect Science, Zhejiang University; Hangzhou 310029, China (Received 12 March 2006; Accepted 25 February 2007)
Abstract Effects of maternal photoperiod on the diapause trait of Cotesia plutellae in two populations, one from Hangzhou (30°14 N), Zhejiang Province, and the other from Changchun (43°52 N), Jilin Province, China, were examined in the laboratory by exposing the mother generation (G0) to 3 day-lengths (8L-16D, 12L-12D, and 16L-8D) at 25°C, and exposing their offspring (G1) to 2 day-lengths (8L-16D, 11L-13D) at 4 temperatures (13, 15, 17, 20°C). All three diapause-inducing factors had a significant influence on the incidence of diapause. Both populations could be induced to enter diapause under pertinent conditions. Long day length in G0 decreased the incidence of diapause and lowered the critical temperature for diapause-induction in G1. There were significant differences in the incidence of diapause between the two populations in almost all combinations. Compared to the southern Hangzhou population, the northern Changchun population produced a higher proportion of diapause individuals, and had higher critical temperatures for diapause-induction in all 6 photoperiod combinations used in G0 and G1 except for the one in which short day length (8L-16D) was used in both generations. Key words: Cotesia plutellae; diapause; geographic variation; maternal effect; photoperiod response
tegrated DBM management (Talekar and Shelton, 1993; Rowell et al., 2005). Since C. plutellae occupies a wide geographical range, theoretically, the diapause attributes regulating its seasonal life cycles should exhibit variation between populations originating from different latitudinal locations. Alvi and Momoi (1994) have observed diapause traits of two geographic populations of C. plutellae, originating from Kuroishi (40.6° N), Aomori Prefecture and Kobe (34°41 N), Hyogo Prefecture, Japan. They found that short photoperiods induced prepupal diapause in the Kuroishi population but did not produce any developmental arrest in the Kobe population when their mother generation was reared under a day length of 16L-8D (16 h light and 8 h darkness) at 20°C. However, they did not observe diapause trait of the Kobe population whose mother generation was maintained under a short day length condition, neither did they make diapause-induction for the Kobe strain at lower temperatures (17°C) with shorter day length
INTRODUCTION Diapause is used to describe the arrested development of insects at a specific stage, and allows insects to survive adverse climatic or environmental conditions (Danks, 1987; Mousseau and Dingle, 1991). Many insects rely on environmental factors as a trigger for the induction of diapause. In the temperate zone, climatic conditions, especially temperature and day length, show clear latitudinal gradients. Therefore, many insects occurring over wide geographical ranges show a latitudinal cline in life history traits as a result of local adaptation (Tauber et al., 1986; Danks, 1987). Cotesia plutellae (Kurdjumov) is a dominant larval parasitoid of the diamondback moth (DBM), Plutella xylostella (L.), which is the most destructive pest on cruciferous crops worldwide. This parasitoid has been registered as a biopesticide (Copping, 1998). In southeast Asian countries, it was also recommended as an optimal component of in-
* To whom correspondence should be addressed at: E-mail:
[email protected] DOI: 10.1303/aez.2007.383
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(9 h per day). If they did so, they would probably have found some diapausing individuals in the Kobe population. In our primary study, we found that C. plutellae originating from Hangzhou (30°14 N), Zhejiang Province, China could be induced to enter diapause under the conditions of 8L16D, 11L-13D at 15°C, and the proportions of diapause ranged from 10 to 30%. In many insects, diapause is influenced by the environmental conditions experienced by the parental generation, in addition to the generation when the diapause occurs. The current study was designed to verify whether the population of C. plutellae from Hangzhou could be induced to enter diapause, to examine the effect of environmental conditions experienced by the mother generation on the incidence of diapause, and to compare the variation in diapause features between the northern and southern populations. MATERIALS AND METHODS Insects and host plants. Two geographic populations of C. plutellae were used in this study. The southern population was collected from brassica fields in the suburbs of Hangzhou (30°14 N), Zhejiang Province, China in May 2003, while the northern population was collected from brassica fields in the suburbs of Changchun (43°52 N), Jilin Province, China in September 2003. Both stock populations originated from about 100 wasp cocoons, and were maintained in the laboratory with the third instar larvae of P. xylostella, which were reared on potted cabbage, Brassica oleracea var. capitata, cv. Jingfeng No. 1, according to the method described by Wang et al. (1999). Both the parasitoid and host insect cultures were reared in temperature-controlled rooms at 25–30°C, 60–80% relative humidity (RH) with a photoperiod of 16L8D. The two parasitoid populations were kept in separate rearing rooms to ensure they were isolated. Parasitoids of both populations used in the experiments were randomly chosen from the stock cultures, fed with 20% honey solution, and were 2–3 day old and mated females. Both populations had been reared for four to seven generations in the laboratory prior to experiments. All observations were carried out in a temperature-controlled room at 25°C, 60–80% RH with light. The rearing method of the wasp for experi-
ments. To obtain larvae parasitized by C. plutellae, one early third instar larva of DBM was provided to one female in a test tube (18 mm diameter, 80 mm in height), and replaced with another one after being stung once by the wasp. Thirty parasitized DBM larvae were placed on a cabbage leaf held in a plastic container. The container was made of a clear plastic cup (110 mm in diameter, 110 mm in height) with holes covered with a fine stainless steel mesh on its top and bilateral walls for ventilation. The cabbage leaf carrying host larvae was fixed to the container base by inserting its petiole through a hole in the base center. The container was placed on top of a 500-ml glass bottle with tap water, and the petiole of the cabbage leaf was kept immersed in water to maintain freshness. The cabbage leaf was replaced as required. Determination of diapause status. The average durations from cocoon formation to adult emergence for non-diapause individuals in cocoons maintained under 15, 17.5, 20, 22.5 and 25°C were 18.5, 9.8, 7.6, 6.1 and 4.4 days, respectively (Shi and Liu, 1999). Based on this relationship of developmental rate (y) over temperature (x) (y0.19090.0163x, r0.9904), and considering the variance among the individuals in developmental duration, the cocoons which failed to produce adult wasps after 56, 24, 13, 10 days under 13, 15, 17 and 20°C, respectively, were dissected under a stereomicroscope and the individuals in the cocoons were classified into three categories: nondiapause individual (pupa or adult), diapause individual (live larvae or prepupa) or dead individual (dead larva, dead prepupa). Since one cocoon contained only one individual, the diapause incidence in this study was calculated using the following formula: % Diapausenumber of cocoons with diapause individuals/(total number of cocoons collectedthe number of cocoons containing dead individuals) Experimental cultures for the induction of diapause. Insects of the maternal generation (G0) were reared from eggs under three day length conditions of 8L-16D, 12L-12D and 16L-8D, respectively at 25°C with ca. 75% RH. No individuals entered diapause under these three conditions due to the high temperature. Their progeny generation
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values was performed by Student’s t-test. All statistical analyses were performed using the statistical software package, STATISTICA (StatSoft., Inc., 2003).
(G1) was reared under eight conditions, comprising of four temperature regimes (13, 15, 17, 20°C) and two photoperiods (8L-16D and 11L-13D), forming 24 treatments in each population. The newly formed G1 cocoons were collected and the numbers of cocoons were recorded daily. The collected cocoons were placed in a test tube (1880 mm length) plugged with cotton and allowed to produce adults or enter larval diapause in the same condition as their egg-larval stage. Finally, the cocoons which failed to produce wasps after the days described above were dissected under a stereomicroscope and individuals in the cocoons were classified into two categories: non-diapause individual or diapause individual. Each treatment for each population was replicated three times and each replicate contained 30 larval individuals. Statistical analysis. The results for the incidence of diapause were statistically examined by analysis of variance (ANOVA) after arcsine transformations, but presented as proportions. Mean values were separated using Tukey’s honestly significantly different (HSD) test when significant differences among several mean values were detected by ANOVA. Comparison between the two mean
RESULTS Response to induction of diapause for Hangzhou population of C. plutellae C. plutellae originating from Hangzhou could be induced to enter diapause (Table 1). The incidences of diapause were observed in 19 of 24 treatments. All three factors (temperature at which G1 was reared, and the photoperiods to which G0 and G1 were exposed) had effects on the incidence of diapause in G1, and significant interactions both between photoperiod experienced by G0 and temperature/photoperiod experienced by G1 and between the temperature and photoperiod in G1 were detected (Table 2). The shorter the photoperiod experienced by G0 and/or by G1 itself and the lower the temperature experienced by G1, the higher the incidences of diapause in the G1 were (Table 1). When G0 was exposed to 16L-8D, and G1 was reared at 17°C or 20°C, no diapausing individuals
Table 1. Larval diapause incidences (meanSE) of Cotesia plutellae in the northern Changchun population (NP) and southern Hangzhou population (SP) under various combinations when maternal generation was reared at 25°C with different photoperiods Incidence of diapause (%) in progeny generationa Mother photoperiod (h)
Progeny temp. (°C)
Progeny under 8L-16D NP
8L-16D 8L-16D 8L-16D 8L-16D 12L-12D 12L-12D 12L-12D 12L-12D 16L-8D 16L-8D 16L-8D 16L-8D a
13 15 17 20 13 15 17 20 13 15 17 20
100.000.0 100.000.0 35.640.88† 18.550.26† 100.000.0 100.000.0† 35.690.72† 9.571.95 100.000.0 27.976.90 10.621.26 1.521.52
Progeny under 11L-13D
SP Aa Aa Ba Ca Aa Aa Ba Ca Aa Bb Bb Cb
95.352.53 45.195.19* 9.440.68* 2.672.67* 70.007.64* 31.336.34*† 5.800.29*† 5.125.12 12.631.45* 5.931.64* 0.000.0* 0.000.0
NP Aa Ba Ca Ca Ab Ba BCb Ca Ac Bb Cc Ca
100.000.0 98.961.04 18.220.65 11.650.67 100.000.0 80.113.58 10.480.33 4.441.36 100.000.0 21.094.64 4.872.54 1.671.67
SP Aa Aa Ba Ba Aa Bb Cab Dab Aa Bc BCb Cb
71.8310.30* 22.916.03* 2.761.56* 5.062.72 43.1317.27* 4.330.79* 0.850.85* 0.000.00* 8.461.56* 0.950.95* 0.000.0 0.000.0
Aa Ba Ba Ba Aab Bb Ba Ba Ab Bb Ba Ba
Means followed by different uppercase letters are significantly different by HSD test (p0.05) among different progeny temperatures under the same mother photoperiod in the same column, while means followed by different lowercase letters are significantly different by HSD test (p0.05) among different mother photoperiods at the same temperature in the same column. Means followed by * indicate the difference between two populations by t-test (p0.05). Means followed by † indicate the difference by t-test (p0.05) when compared with the same population but reared under a photoperiod of 11L-13D.
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U. A. M. AHMED et al. Table 2. Three-way analysis of variance testing the effect of the environmental conditions experienced by maternal generation (G0) and by progeny generation (G1) on diapause incidence in progeny larvae of Cotesia plutellae in the northern Changchun population and southern Hangzhou population
Degrees of freedom
Effect
Photoperiod in G0 (A) Temperature in G1 (B) Photoperiod in G1 (C) AB AC BC ABC Error a
2 3 1 6 2 3 6 48
Southern Hangzhou population
Northern Changchun population
Mean squares
Fa
Mean squares
Fa
3,643.4 6,534.5 1,550.0 558.0 169.6 202.2 37.5 52.9
68.84** 123.46** 29.28** 10.54** 3.20** 3.82* 0.71
3,611.7 22,609.0 838.9 1,092.0 134.1 158.7 46.5 14.8
243.34** 1,523.28** 56.52** 73.57** 9.04** 10.69** 3.13*
Asterisks indicate probability levels (** p0.01, * p0.05). Table 3. Four-way analysis of variance testing the effect of the environmental conditions experienced by maternal generation (G0) and by progeny generation (G1) on diapause incidence in progeny larvae of Cotesia plutellae in the northern Changchun population and southern Hangzhou population
a
Effect
Degrees of freedom
Mean squares
Fa
Population (P) Photoperiod in G0 (A) Temperature in G1 (B) Photoperiod in G1 (C) PA PB PC AB AC BC PAB PAC PBC ABC PABC Error
1 2 3 1 2 3 1 6 2 3 6 2 3 6 6 96
29,492.6 7,175.9 26,375.0 2,334.7 79.2 2,768.5 54.2 626.1 258.5 192.2 1,023.9 15.1 168.8 42.4 41.6 33.9
870.35** 211.77** 778.35** 68.90** 2.34 81.70** 1.60 18.48** 8.52** 5.67** 30.22** 0.45 4.98** 1.25 1.23
Asterisks indicate probability levels (** p0.01).
were found as reported by Alvi and Momoi (1994). Maternal effect of photoperiod on the incidence of larval diapause in C. plutellae The photoperiod experienced by G0 had a significant influence on the larval diapause incidence of C. plutellae in G1 (Tables 2 and 3). A long photoperiod in G0 lowered the critical temperature (at which 50% individuals entered diapause) for diapause induction in both populations (Table 4). However, the influence on the two populations was
different (Table 3, see interaction between population and temperature in G1). When wasps in G1 were reared at 13°C, all individuals in the northern Changchun population entered diapause regardless of the photoperiod experienced by both their mothers and themselves, but the incidence of diapause in the southern Hangzhou population decreased significantly with increase of the photoperiod experienced by their mothers. When C. plutellae in G1 was reared at 15°C or above, in the northern Changchun population, the
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Table 4. The critical temperature regimes (°C) for diapause induction of Cotesia plutellae in the northern Changchun population (NP) and southern Hangzhou population (SP) under various photoperiod combinations in both parental and progeny generations Critical temperature regimesa (°C) Photoperiod by mother at 25°C
8L-16D 8L-16D 12L-12D 12L-12D 16L-8D 16L-8D a
Photoperiod in progeny
8L-16D 11L-13D 8L-16D 11L-13D 8L-16D 11L-13D
NP
SP
15–17 15–17 15–17 15–17 13–15 13–15
15–17 13–15 13–15 13 13 13
50% individuals entered diapause at the temperature regimes.
longer photoperiod experienced by G0 still produced significantly lower incidence of diapause in G1 than the shorter photoperiods did; while in the southern Hangzhou population, the influence of photoperiod experienced by G0 was exhibited only in G1 under 8L-16D at temperatures of 17°C and lower. Variation in diapause feature between two populations The northern Changchun population demonstrated an equal or higher incidence of diapause in all combinations than the southern Hangzhou population, and a significant difference between the two populations was detected in 18 of 24 combinations (Table 1). The critical temperature for diapause induction in the southern Hangzhou population was lower than that in the northern Changchun population with an exception when C. plutellae in both generations was reared under the photoperiod of 8L-16D (Table 4). At lower temperatures (13°C and 15°C), the diapause incidence was more easily effected by the photoperiod experienced by the G0 in the southern Hangzhou population than in the northern Changchun population; while at higher temperatures (17°C and 20°C), the diapause incidence was more readily affected by the photoperiod experienced by the G1 in the northern Changchun population than in the southern Hangzhou population, although the incidences of diapause in both populations did not exceed 50%. DISCUSSION C. plutellae originating from Hangzhou could be
induced to enter diapause. This result is not consistent with Alvi and Momoi (1994), who reported that a short photoperiod did not produce any developmental arrest in Kobe strain (34°41 N) of C. plutellae. Compared with the Kobe strain, the Hangzhou population (30°14 N) of C. plutellae used in our study is more southern in latitudinal origin. From their report, we guess they did not expose the Kobe strain of C. plutellae to conditions at lower temperature (15°C or 13°C) and shorter photoperiod (8L-16D), although such a short day length would never occur naturally in either Kobe or Hangzhou. Based on our results, it could be inferred that if they reared G0 under a shorter photoperiod (12L-12D or shorter), they would find that the Kobe strain could also be induced to enter diapause, and the incidence of diapause under some conditions would be quite high. Short day length in the parental generation has a diapause-inducing effect in C. plutellae. This phenomenon has been reported for many other insects and mites (Mousseau and Dingle, 1991; Rockey et al., 1991; McWatters and Saunders, 1997, 1998; Webb and Denlinger, 1997; Milonas and Savopoulou-Soultani, 2000; Vinogradova and Reznik, 2002; Oku et al., 2003; Tachibana and Numata, 2004). Although the parental phenotypic plasticity adjusts offspring phenotypes in order to accommodate offspring to predictable future environments (Mousseau and Fox, 1998), the temperature and photoperiod experienced by the offspring were still two key factors determinating the incidence of diapause in C. plutellae. For multivoltine insects, the mother, by using the experienced photoperiod, may “predict”, at least to some extent,
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changes in environment in their offspring, and produce some signals, which could be transferred through the cytoplasm to offspring. Their offspring could thus enter diapause when adverse conditions appear, or develop when favorable ones occur. This strategy, in which the maternal generation only partially determines the tendency whether their progeny would enter diapause or not, or in other words that the diapause incidence would be determined jointly by their mother and themselves, may be another kind of risk-spreading or bet-hedging strategy like that seen in the egg-diapause ground cricket, Allonemobius socius, of which the firstgeneration females could lay mixtures of direct-developing and diapause eggs to ensure that at least some progeny will be suited for unpredictable future conditions (Bradford and Roff, 1997; Hopper, 1999). The multiplicity of factors involved in 2 generations for diapause initiation is considered an adaptation of multivoltine species with a short development time, permitting the parasitoid to adequately assess seasonal changes in the environment (Brodeur and McNeil, 1989). Other conditions experienced by mother, such as temperature and interaction between temperature and photoperiod, may also have an influence on the incidence of diapause in C. plutellae, but the influence of such conditions still remains to be investigated in the future. The northern Changchun population produced a higher incidence of diapause and had a higher critical temperature for diapause induction in most of the tested combinations than the southern Hangzhou population. Such variability in diapause trait between populations for most widespread insect and mite species has been well documented (Maslennikova and Mustafayeva, 1971; Weseloh, 1982; Brodeur and McNeil, 1989; Kraaijeveld and Alphen, 1995; McWatters and Saunders, 1996; Yoshio and Ishii, 1998; Ito and Nakata, 2000; Shimizu and Kawasaki, 2001; Kurota and Shimada, 2003; Gillespie and Quiring, 2005; Kato, 2005; Schmidt et al., 2005; Takafuji et al., 2005). The differences reflect physiological and ecological adaptations to local climatic conditions. Day lengths are longer but the climate is colder between the spring and autumn equinoxes at higher latitudes than at lower latitudes, and the summer ends early with longer day length at higher latitudes compared to that at lower latitudes. This means that changes in photoperiod and temperature occur much more
quickly at higher latitudes than at lower latitudes, and therefore, the northern Changchun population will face severe climatic conditions sooner than the southern Hangzhou population. Any organism which wants to distribute in such a severe climatic condition has to develop some strategies to adapt to it. Diapause and migration are two ways for an organism to cope with the adverse conditions; both ways could avoid the inclement seasons and make full use of the favorable seasons. However, there is no published evidence that C. plutellae could make a long distance migration from southern to northern area, although the diamondback moth does (Honda, 1990). The higher diapause incidence and the higher critical diapause-inducing temperature in the northern Changchun population are consequences of physiological and ecological adaptations to local climatic conditions. ACKNOWLEDGEMENTS This study was funded by the National Basic Research Program of China (973 Program) (No. 2006CB102005) and National Natural Science Foundation of China (Project 30170627).
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