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Article

Adaptability of the Soybean Aphid Aphis glycines (Hemiptera: Aphididae) to Temperature and Photoperiod in a Laboratory Experiment

by
Bo Gao
1,2,†,
Kaice Yang
1,
Yifan Tian
1,
Bing Bai
1,3,
Zhenqi Tian
1,† and
Jian Liu
1,*
1
College of Plant Protection, Northeast Agricultural University, Harbin 150030, China
2
Graduate School of Chinese Academy of Agricultural Sciences, Chinese Academy of Agricultural Sciences, Beijing 100081, China
3
Key Laboratory of Economic and Applied Entomology of Liaoning Province, College of Plant Protection, Shenyang Agricultural University, Shenyang 110866, China
*
Author to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Insects 2024, 15(10), 816; https://doi.org/10.3390/insects15100816
Submission received: 12 September 2024 / Revised: 12 October 2024 / Accepted: 12 October 2024 / Published: 17 October 2024
(This article belongs to the Section Insect Physiology, Reproduction and Development)
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Simple Summary

The soybean aphid, Aphis glycines, is a crucial soybean pest, which has two major hosts, cultivated and wild soybean. This study mainly proved that the A. glycines fed on wild soybean exhibited significant differences in morph differentiation, temperature adaptability, and photoperiod adaptability, compared with the A. glycines fed on cultivated soybean. It is important to understand the life cycle of A. glycines in Harbin, northeast China, and formulate an integrated pest management strategy for A. glycines in the region.

Abstract

The soybean aphid, Aphis glycines Matsumura, 1917, is a crucial soybean pest. Cultivated soybean, Glycine max (Carl von Linné) Elmer Drew Merrill, 1917, and wild soybean, Glycine soja Philipp Franz von Siebold & Joseph Gerhard Zuccarini, 1843, are summer hosts of A. glycines. In this study, the development, reproduction, and morphogenesis of A. glycines fed wild soybean (AgFW) were studied at different temperatures and photoperiods. The data were compared with that of A. glycines fed soybean (AgFS). At 20–29 °C, the adult lifespan of the first–third-generation AgFW was shorter than or equal to that of AgFS. Significant differences existed in the adult fecundity and intrinsic rate of increase between AgFW and AgFS. At a 10L:14D h photoperiod, males of AgFW were deposited earlier than, or as early as, males of AgFS. At 17 °C, the gynoparae of AgFW were deposited in proportions greater than or equal to those of AgFS. Based on these results, we concluded that the adaptability of AgFW and AgFS to temperature and photoperiod significantly differs. It is important to understand the life cycle of A. glycines in Harbin, northeast China, and formulate an integrated pest management strategy for A. glycines in the region.

1. Introduction

The soybean aphid, Aphis glycines Matsumura, 1917, is a crucial soybean pest native to Asia. Aphis glycines is a species with an expanding range, which is acquiring new territories, including North America. After 2000, A. glycines invaded North America and spread rapidly throughout the region [1]. The life cycle of A. glycines is heteroecious and holocyclic (host alternating with sexual reproduction during part of its life cycle) [2,3]. In summer, A. glycines virginoparae colonize cultivated soybean, Glycine max (Carl von Linné) Elmer Drew Merrill, 1917, and reproduce parthenogenetically throughout the season [4,5]. As the temperature decreases and the photoperiod shortens in autumn, gynoparae, males, and oviparae of A. glycines are deposited [1,6]. Soybeans infested with A. glycines display leaf shrinkage, internode shortening, plant dwarfing, and reduced pod number [7]. Through direct feeding [2] and indirect damage by virus transmission [8,9], A. glycines has caused up to 30% yield loss in soybeans during certain years with heavy infestations [7].
The morphological characteristics, population dynamics, and natural enemies of A. glycines have been studied in various regions [10,11,12,13,14,15,16]. The economic threshold used in A. glycines management is 250 aphids per plant [17,18]. In the control of this pest, insecticides [19,20,21], seed treatment [22], and gene silencing [23] have been applied. The natural control of A. glycines was mainly resistant plants, natural enemy insects, and microorganisms, which were reported in previous studies [5,15,16]. The adaptability of A. glycines to constant day–night and fluctuating temperatures has been studied [24,25,26,27]. At day–night constant temperatures ranging from 13 to 33 °C, A. glycines nymphs developed into adults [28]. At a constant 35 °C, A. glycines nymphs did not develop into adults, and all died within 8 d [29]. The population growth rates of A. glycines were greatest at 25 °C, with the aphid population doubling in size in 1.5 days [25]. At diurnal 35 °C and nocturnal 20 °C, a few nymphs of A. glycines developed into adults; however, few offspring were deposited [27].
Cultivated soybean, G. max, and wild soybean, Glycine soja Philipp Franz von Siebold & Joseph Gerhard Zuccarini, 1843, are summer hosts of A. glycines [5]. A few studies focused on the characteristics of A. glycines fed wild soybeans (AgFW). In summer, A. glycines colonize cultivated soybeans; however, a few A. glycines are observed on wild soybeans. On the contrary, A. glycines colonize wild soybeans in autumn; however, a few A. glycines also colonize cultivated soybeans in autumn. Based on the aforementioned phenomena, the occurrence and feeding hosts of AgFW and A. glycines fed soybeans (AgFS) differ. The latest research results showed that AgFW was significantly more affected than AgFS by heat waves lasting for 7 d, which reduced the adult reproductive ability and male differentiation proportion in the offspring of A. glycines [30]. The phenomena and the research results mentioned above led us to infer that the adaptability of AgFW to temperature and photoperiod is probably different than that of AgFS.
This study investigated the development and reproduction of AgFW in three generations at different temperatures and the morphogenesis at different temperatures and photoperiods, and the data were compared with that of AgFS. AgFW and AgFS were fed on cultivated soybeans and wild soybeans, respectively. They had been reared on a non-original nutritional diet, and the development and reproduction of the aphids were also studied and compared. This information is important for understanding the life cycle of A. glycines in Harbin. In regions where AgFW occurs, critical questions regarding soybean production remain unanswered. For example, whether AgFW reproduction results in more gynoparae and males than AgFS reproduction. The results of the morph differentiation in AgFW are important for formulating integrated pest management strategies for A. glycines in regions where G. soja is common.

2. Materials and Methods

2.1. Aphid and Hosts

Apterous AgFS were collected at a cultivated soybean field in Northeast Agricultural University, Harbin (126.72° E, 45.74° N), northeast China, in July 2018. Apterous AgFW were collected in September 2018 from an area where wild soybeans grow on Sun Island (126.58° E, 45.79° N), Harbin, where no cultivated soybeans were planted. The population of AgFS was maintained on cultivated soybean seedlings (variety Heinong 51). The population of AgFW was maintained on wild soybean plants, which were both asexually reared in growth chambers at 25 ± 1 °C, 70 ± 5% relative humidity (RH), and a photoperiod of 14L:10D-h with artificial light of 12,000 lux. To maintain AgFS and AgFW, 20–30 aphids each were transferred from mature, heavily infested plants to young, non-infested plants every 2 weeks.
Cultivated soybean seeds (Heinong 51) were purchased from Fangyuan Agricultural Co., Ltd., Wuchang, Heilongjiang Province, China. The cultivated soybean seedlings were planted in circular plastic pots (d × h: 10 × 10 cm). Six to eight cultivated soybean seeds were planted in each pot and placed in a growth chamber. The conditions in the growth chamber were set at 25 ± 1 °C, 70 ± 5% RH, and 14L:10D-h photoperiod with artificial light of 12,000 lux. Cultivated soybean seedlings of 15–20 cm (V2–V3 developmental stage) were used in the experiment. Wild soybean seeds were collected from a wild soybean-growing area on Sun Island. Wild soybeans were planted in plastic pots in a chamber under the same conditions. The seed coat of wild soybeans is thick and hard, which is not conducive to germination. To increase the emergence, we removed parts of the thick testa of the seeds using a knife before planting. Wild soybeans were used for the experiments after 27 days of growth (at florescence) and sprouting.

2.2. Development and Reproduction of AgFS and AgFW in Three Generations

Fifty apterous AgFS and AgFW adults were placed in five pots (10 aphids per pot) of soybeans and wild soybeans, respectively. The plants were placed in a growth chamber at 25 ± 1 °C and 70 ± 5% RH, and a 14L:10D-h photoperiod with artificial light of 12,000 lux for a 24 h reproductive period; thereafter, all adults were removed. Newly deposited nymphs (recorded as G1) were removed from plants using a small brush. AgFS and AgFW nymphs were transferred to cultivated soybeans and wild soybeans, respectively, and reared individually using the moisturizing cotton method. In brief, a piece of square moisturizing cotton (Shenzhen Xide E-commerce Co., Ltd, Shenzhen, China) (facial cleansing cotton; l × w × h: 2 × 2 × 0.4 cm) was placed on the bottom of a 45 mL, 4 × 4.5 cm (d × h) glass beaker, and a piece of round filter paper with a 4.2 cm diameter was placed on the surface of the moisturizing cotton. The filter paper was cut slightly larger to fix it firmly within the beaker. The filter paper and moisturizing cotton were then wetted with 2200 μL of water by dropping water onto the surface of the filter paper with a pipette. Detached leaves of G. max and G. soja were cut into 1.5 cm2 square pieces using scissors. Each nymph was placed on the reverse side of a square leaf adhered to a filter paper surface. A small drop of water was placed on the surface of the filter paper, and a square piece of leaf was placed on the surface. Due to the application of slight pressure using a small brush, the leaf adhered to the filter paper because of the surface tension of the water. Water was added to the surface of the filter paper every 7–10 d (400 μL each time). The leaves were replaced every 5–7 d or when they became yellowish [27,31].
When G1 developed into adults, newly deposited nymphs (G2) were placed and reared on soybeans and wild soybeans. When G2 developed into adults, newly deposited nymphs (G3) were reared on each host. The G1, G2, and G3 groups were reared individually using the moisturizing cotton method. AgFS and AgFW were reared on cultivated soybeans and wild soybeans, respectively. Nymphs were placed in growth chambers at 20, 23, 26, and 29 ± 1 °C and 70 ± 5% RH, and the photoperiod was 14L:10D-h with artificial light of 12,000 lux. Each aphid was considered an experimental unit, and 50 AgFS and AgFW nymphs were used for each temperature treatment. Individual nymphs were examined daily for exuviation and survival. Once they developed into adults, the nymphs deposited by each female were counted and removed daily. The adult lifespan was recorded daily until the death of each adult [28].

2.3. Development and Reproduction of AgFS on Wild Soybean and AgFW on Soybean

To investigate the differences in the development and reproduction of AgFS and AgFW on a non-original nutritional diet, we changed the feed: AgFS was fed wild soybeans, and AgFW was fed cultivated soybeans. Each aphid was considered an experimental unit, and 50 newly deposited AgFS and AgFW nymphs were used for each temperature treatment. The nymphs were individually reared using the moisturizing cotton method and placed in growth chambers at 17, 20, 23, 26, 29, or 32 ± 1 °C, 70 ± 5% RH, with a 14L:10D-h photoperiod. Individual nymphs were examined daily for exuviation and survival. Once they developed into adults, the nymphs deposited by each female were counted and removed daily. The adult lifespan was recorded daily until the death of each adult [28].

2.4. Morph Differentiation of AgFS and AgFW at Different Temperatures and Photoperiods

The temperature and photoperiod combination treatments were set as follows: (1) four temperatures of 17, 20, 23, and 26 ± 1 °C, with a photoperiod of 10L:14D h and 70 ± 5% RH; and (2) three photoperiods of 8:16, 12:12, and 16:8 (L:D) h, with 17 ± 1 °C and 70 ± 5% RH. For each treatment, 20 apterous adults of AgFS and 50 apterous adults of AgFW (recorded as F0) were first reared at 25 ± 1 °C and 70 ± 5% RH with a 14L:10D h photoperiod. Under these conditions, the adult fecundity of AgFS per day was approximately 5–6 offspring per female, and that of AgFW was approximately 2–3 offspring per female. Thus, the number of offspring deposited by 20 AgFS adults per day was similar to that of 50 AgFW adults. After 24 h, the adults were removed, and newly deposited nymphs (recorded as F1) were reared in each treatment. When F1 developed into adults, the nymphs deposited on days 1, 6, 11, 16, and 21 (F2) were reared under the same conditions as aforementioned [26]. All nymphs and adults were reared individually using the moisturizing cotton method. AgFS were reared with cultivated soybeans, and AgFW were reared with wild soybeans. When the F2 developed into adults, they were identified as virginoparae, gynoparae, and males based on their morphological characteristics [11]. The proportions of the different morphs that occurred on days 1, 6, 11, 16, and 21 were recorded. Three replicates were performed for each group.

2.5. Data Analyses

The nymph stage duration, adult lifespan, and adult fecundity of AgFS and AgFW were calculated according to Chi and Liu 1985 and Chi 1988 [32,33] using TWOSEX-MSChart software (Version number, 2019.06.07) [34]. The intrinsic rate of increase in AgFS and AgFW were calculated by bootstrap technology using the TWOSEX-MSChart [35]. Bootstrap technology with 100,000 resamplings were used to estimate the variances and standard errors [36]. When AgFS was fed cultivated soybean and AgFW was fed wild soybean for three generations, after which the feeds were switched for one generation, the differences in nymph stage duration, adult lifespan, adult fecundity, and intrinsic rate of increase between AgFS and AgFW at each generation and temperature, and the differences in the parameters between AgFS and AgFW at each temperature, were analyzed by a paired bootstrap test (TWOSEX-MSChart) [37].
The percentages of virginoparae, gynoparae, and males in AgFS and AgFW were determined and transformed to arcsine square-root values to fit the normal distribution. Transformed values were used for data analysis. The differences in the percentage of each morph deposited in F2 on days 1, 6, 11, 16, and 21 between AgFS and AgFW at each temperature and photoperiod treatment were analyzed using Student’s t test (SAS 8.1).

3. Results

3.1. Development and Reproduction of AgFS and AgFW

At 20 °C and 26 °C, the nymph stage durations of the first, second, and third generation AgFW were shorter than or equal to those of AgFS (Figure 1a,c). At 23 °C, the nymph stage duration of the first, second, and third generation AgFW was longer than or equal to that of AgFS (Figure 1b). At 20–26 °C, the adult lifespan of the first, second, and third generation AgFW was shorter than or equal to that of AgFS (Figure 1e–g). At 29 °C, the adult lifespan of the first generation AgFW was shorter than that of AgFS. The adult lifespan of the second generation of AgFW was as long as that of AgFS (Figure 1h).
At 20–29 °C, significant differences existed in adult fecundity and intrinsic rate of increase between AgFW and AgFS of the first, second, and third generation (Figure 2c,g) or certain generations (Figure 2a,b,d,e,f,h). In addition, there were significant differences in biological parameters among different treatments under different temperatures, generations, or populations (Tables S1 and S2).
To investigate the performance of AgFW on the non-origin host, AgFW were reared on cultivated soybeans. At 17 °C to 32 °C, AgFS and AgFW developed and reproduced successfully on wild and cultivated soybean; however, certain significant differences existed in the nymph stage duration, adult lifespan (Table 1 and Table S3), adult fecundity, and intrinsic rate of increase between AgFS and AgFW (Table 2 and Table S4). At 17 °C, AgFW fed on soybean had a longer nymph stage duration and adult lifespan (Table 1).

3.2. Morph Differentiation of AgFS and AgFW at Different Temperatures and Photoperiods

At 17 °C and a 10L:14D-h photoperiod, on day 1, a higher percentage of gynoparae (Figure 3a) and a lower percentage of virginoparae of AgFW (Figure 3i) were deposited than that of AgFS. At 20 °C and a 10L:14D-h photoperiod, on days 1, 6, 11, 16, and 21, the percentages of gynoparae (Figure 3b), males (Figure 3f), and virginoparae (Figure 3j) deposited by AgFW were equal to those of AgFS. At 23 °C and a 10L:14D-h photoperiod, on days 1 and 6, males were deposited by AgFW. No males were deposited by AgFS (Figure 3g). On day 11, a smaller percentage of gynoparae of AgFW (0.74 ± 0.74%) was deposited than that of AgFS (14.49 ± 2.84%) (Figure 3c). At 26 °C and a 10L:14D-h photoperiod, AgFW deposited gynoparae on day 1 (Figure 3d) and males on day 6 (Figure 3h). The offspring deposited by AgFS on days 1–6 were virginoparae (Figure 3l). On day 21, the offspring treated with AgFW were all virginoparae (Figure 3l), and the offspring treated with AgFS were male (Figure 3h) and virginoparae (Figure 3l).
At 17 °C and an 8L:16D-h photoperiod, on day 6, a higher percentage of gynoparae (Figure 4a) and lower percentage of males (Figure 4d) were deposited by AgFW than by AgFS. At 17 °C and a 12L:12D-h photoperiod, on days 1 and 16, a higher percentage of gynoparae (Figure 4b) and males (Figure 4e) were deposited by AgFW than that by AgFS. A lower percentage of virginoparae of AgFW was deposited on days 1–16 than that of AgFS (Figure 4h). At 17 °C and a 16L:8D-h photoperiod, on days 1 and 6, the percentages of AgFW gynoparae were higher than those of AgFS (Figure 4c). On days 1 to 21, a higher percentage of males (Figure 4f) and a lower percentage of virginoparae (Figure 4i) were deposited by AgFW than by AgFS. In addition, there were significant differences in percentage of gynoparae or male of AgFW and AgFS at each temperatures or photoperiods (Tables S5 and S6).

4. Discussion

Previous studies proved that aphids could have different host-specialized biotypes [38]. In A. gossypii, non-original hosts led to aphid death and even population collapse [39,40]. However, these phenomena were not observed in A. glycines. When AgFS and AgFW were transferred to rearing on the non-original host, both developed into adults and were successfully reproduced (Table 1 and Table 2). Therefore, we concluded that AgFW has probably not evolved a wild soybean-specialized biotype in soybean aphids. However, more evidence for the identification of a wild soybean-specialized biotype should be conducted in other natural populations of A. glycines collected from wild soybean.
This study is the first to report on AgFW regarding the temperature and photoperiod set in trials. The development, reproduction, and morphogenesis of AgFS have been studied in previous studies, and the data are comparable. AgFS can survive and maintain a population on cultivated soybean at a temperature range from 20 to 29 °C (Figure 1 and Figure 2), which is consistent with studies focused on the effect of temperature on a single generation of A. glycines [25,41,42]. At 29 °C, the nymph stage duration and adult longevity of AgFS (Figure 1) were similar to those of another study [42]. At 20 °C, the adult fecundity of the first-generation AgFS (Figure 2) was lower than the reported result, 63.5 ± 2.2 offspring per female [25]; however, it was higher than the reported 27.87 ± 15.64 offspring per female [41]. The performance of A. glycines in development and reproduction was affected by the rearing method [31] and the different populations of A. glycines used in other studies [43]. In our study, A. glycines were collected from Harbin, China, and reared using the moisturizing cotton method. The differences in the adult fecundity of A. glycines among the studies could be partially attributed to the different rearing methods and origins of the A. glycines used. At low temperatures and short photoperiods, gynoparae and males of AgFS and AgFW were deposited (Figure 3 and Figure 4), which is consistent with the literature on A. glycines fed on cultivated soybeans [26,44,45].
At a 10L:14D h photoperiod and 23 °C, males were deposited by AgFW on days 1–6. However, no gynoparae (the morph producing oviparae) were deposited (Figure 3). This phenomenon is probably protective in AgFW. This result is inconsistent with the reported life cycle of A. glycines, in which gynoparae occur earlier than males and migrate to winter hosts to produce oviparae [2]. The males deposited by AgFW might act as explorers in searching for winter hosts in the life cycle of A. glycines, which occurs earlier in the field, and then migrates to winter hosts where they wait for oviparae. When the oviparae develop into adults, the males can mate with them. If males of A. glycines occur later than oviparae in nature, oviparae must wait for males on the winter hosts, which would cause a high risk of pre-reproductive death and hinder population breeding. Thus, the AgFW is probably an important component of the A. glycines life cycle, which has been neglected until now. A low temperature and short photoperiod combination is commonly observed in September in Harbin. Therefore, the results of the morph differentiation of AgFW at 23 °C and 10L:14D-h can reflect what would be observed in nature to a certain extent. Global warming is an indisputable phenomenon. Heilongjiang Province in northeast China is one of the regions experiencing a rapid temperature increase [46]. In regions with rising environmental temperatures, native organisms are experiencing increased survival pressures. As global warming intensifies in Harbin, Heilongjiang Province, temperatures of 26 °C in autumn with a short photoperiod might occur. In autumn at 26 °C and a 10L:14D h photoperiod, males and gynoparae probably will be deposited by AgFW earlier in the field than by AgFS, as was presented in the laboratory (Figure 3). With its reproductive adaptability strategy, A. glycines is likely to continue to flourish in Harbin, northeast China, where the local environmental temperature is increasing.
Wild soybeans are regarded as important farmland weeds when grown in large numbers in soybean fields, which would result in reduced production [47,48]. Our study showed that the males and gynoparae of AgFW are deposited earlier than usual or in large proportions, which helps A. glycines to complete its life cycle. The larger autumn populations of A. glycines would probably lead to an excessive summer population that would damage cultivated soybean in the following year. Thus, measures to eradicate wild soybeans around cultivated soybean is important for the integrated management of A. glycines in the field, which would probably reduce the numbers of A. glycines gynoparae and males occurring in autumn to some extend. However, our study had some limitations in exploring the adaptability of the different populations of AgFW, which were collected from different wild soybeans in nature. More populations of AgFW would improve our understanding of A. glycines fed on wild soybean. Be that as it may, our work provides an important understanding of the adaptability of A. glycines to temperature and photoperiod in the laboratory, perfecting the life cycle of A. glycines in Harbin, northeast China.

5. Conclusions

Our study confirmed that the temperature adaptability between AgFS and AgFW was significantly different under multiple generations. We further demonstrated that the morph differentiation of AgFW performed differently from AgFS in various temperature and photoperiod conditions. These results suggested that AgFW had significant differences in morph differentiation, temperature adaptability, and photoperiod adaptability, compared with AgFS. It is crucial to understand the life cycle of A. glycines fed on different hosts in Harbin, northeast China, and provide a sound foundation for developing insect control strategies.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/insects15100816/s1, Table S1: Under different analysis modes, the nymph stage duration and adult longevity of AgFS on soybean and AgFW on wild soybean at different generations; Table S2: Under different analysis modes, the adult fecundity and intrinsic rate of increase of AgFS on soybean and AgFW on wild soybean at different generations; Table S3: Under different analysis modes, nymph stage duration and adult lifespan of AgFS on wild soybean and AgFW on soybean;.Table S4: Under different analysis modes, adult fecundity and intrinsic rate of increase of AgFS on wild soybean and AgFW on soybean; Table S5: The difference analysis of the percentage of gynoparae of A. glycines at each temperatures; Table S6: The difference analysis of the percentage of gynoparae of A. glycines at each photoperiod.

Author Contributions

Conceptualization, B.G., Z.T. and J.L.; methodology, B.G., B.B. and Z.T.; software, B.B. and Z.T.; validation, K.Y. and Y.T.; formal analysis, B.G., B.B. and Z.T.; investigation, B.G. and Z.T.; writing—original draft preparation, B.G., K.Y., Y.T. and B.B.; writing—review and editing, Z.T. and J.L.; funding acquisition, J.L. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the Postdoctoral Scientific Research Developmental Fund of Heilongjiang Province, China (LBH-Q15015) and a construction project of a radar monitoring station for migratory pests in Heilongjiang Province.

Data Availability Statement

Data will be made available on request.

Conflicts of Interest

The authors declare no conflicts of interest.

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Insects 15 00816 g001
Figure 1. Nymph stage duration and adult longevity of AgFS on soybean and AgFW on wild soybean at different generations. (a) Nymph stage duration of AgFS and AgFW at 20 °C. (b) Nymph stage duration of AgFS and AgFW at 23 °C. (c) Nymph stage duration of AgFS and AgFW at 26 °C. (d) Nymph stage duration of AgFS and AgFW at 29 °C. (e) Adult longevity of AgFS and AgFW at 20 °C. (f) Adult longevity of AgFS and AgFW at 23 °C. (g) Adult longevity of AgFS and AgFW at 26 °C. (h) Adult longevity of AgFS and AgFW at 29 °C. The data are shown as the mean ± SE. The differences in nymph stage duration or adult longevity between AgFS and AgFW at each generation are marked with ‘*’ (paired bootstrap test, p < 0.05).
Figure 1. Nymph stage duration and adult longevity of AgFS on soybean and AgFW on wild soybean at different generations. (a) Nymph stage duration of AgFS and AgFW at 20 °C. (b) Nymph stage duration of AgFS and AgFW at 23 °C. (c) Nymph stage duration of AgFS and AgFW at 26 °C. (d) Nymph stage duration of AgFS and AgFW at 29 °C. (e) Adult longevity of AgFS and AgFW at 20 °C. (f) Adult longevity of AgFS and AgFW at 23 °C. (g) Adult longevity of AgFS and AgFW at 26 °C. (h) Adult longevity of AgFS and AgFW at 29 °C. The data are shown as the mean ± SE. The differences in nymph stage duration or adult longevity between AgFS and AgFW at each generation are marked with ‘*’ (paired bootstrap test, p < 0.05).
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Figure 2. Adult fecundity and intrinsic rate of increase of AgFS on soybean and AgFW on wild soybean at different generations. (a) Adult fecundity of AgFS and AgFW at 20 °C. (b) Adult fecundity of AgFS and AgFW at 23 °C. (c) Adult fecundity of AgFS and AgFW at 26 °C. (d) Adult fecundity of AgFS and AgFW at 29 °C. (e) Intrinsic rate of increase of AgFS and AgFW at 20 °C. (f) Intrinsic rate of increase of AgFS and AgFW at 23 °C. (g) Intrinsic rate of increase of AgFS and AgFW at 26 °C. (h) Intrinsic rate of increase of AgFS and AgFW at 29 °C. The data are shown as the mean ± SE. The differences in adult fecundity and intrinsic rate of increase between AgFS and AgFW at each generation are marked with ‘*’ (paired bootstrap test, p < 0.05).
Figure 2. Adult fecundity and intrinsic rate of increase of AgFS on soybean and AgFW on wild soybean at different generations. (a) Adult fecundity of AgFS and AgFW at 20 °C. (b) Adult fecundity of AgFS and AgFW at 23 °C. (c) Adult fecundity of AgFS and AgFW at 26 °C. (d) Adult fecundity of AgFS and AgFW at 29 °C. (e) Intrinsic rate of increase of AgFS and AgFW at 20 °C. (f) Intrinsic rate of increase of AgFS and AgFW at 23 °C. (g) Intrinsic rate of increase of AgFS and AgFW at 26 °C. (h) Intrinsic rate of increase of AgFS and AgFW at 29 °C. The data are shown as the mean ± SE. The differences in adult fecundity and intrinsic rate of increase between AgFS and AgFW at each generation are marked with ‘*’ (paired bootstrap test, p < 0.05).
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Figure 3. Percentage of different A. glycines morphs deposited in the F2 when the F1 of AgFS and AgFW was exposed to different temperatures with a photoperiod of 10L:14D. (a) Gynoparae percentage of AgFS and AgFW at 17 °C. (b) Gynoparae percentage of AgFS and AgFW at 20 °C. (c) Gynoparae percentage of AgFS and AgFW at 23 °C. (d) Gynoparae percentage of AgFS and AgFW at 26 °C. (e) Male percentage of AgFS and AgFW at 17 °C. (f) Male percentage of AgFS and AgFW at 20 °C. (g) Male percentage of AgFS and AgFW at 23 °C. (h) Male percentage of AgFS and AgFW at 26 °C. (i) Virginoparae percentage of AgFS and AgFW at 17 °C. (j) Virginoparae percentage of AgFS and AgFW at 20 °C. (k) Virginoparae percentage of AgFS and AgFW at 23 °C. (l) Virginoparae percentage of AgFS and AgFW at 26 °C. The data are shown as the mean ± SE. The differences in percentage of gynoparae, males, or virginoparae between AgFS and AgFW at days 1, 6, 11, 16, and 21 are marked with ‘*’ (Student’s t-test, p < 0.05).
Figure 3. Percentage of different A. glycines morphs deposited in the F2 when the F1 of AgFS and AgFW was exposed to different temperatures with a photoperiod of 10L:14D. (a) Gynoparae percentage of AgFS and AgFW at 17 °C. (b) Gynoparae percentage of AgFS and AgFW at 20 °C. (c) Gynoparae percentage of AgFS and AgFW at 23 °C. (d) Gynoparae percentage of AgFS and AgFW at 26 °C. (e) Male percentage of AgFS and AgFW at 17 °C. (f) Male percentage of AgFS and AgFW at 20 °C. (g) Male percentage of AgFS and AgFW at 23 °C. (h) Male percentage of AgFS and AgFW at 26 °C. (i) Virginoparae percentage of AgFS and AgFW at 17 °C. (j) Virginoparae percentage of AgFS and AgFW at 20 °C. (k) Virginoparae percentage of AgFS and AgFW at 23 °C. (l) Virginoparae percentage of AgFS and AgFW at 26 °C. The data are shown as the mean ± SE. The differences in percentage of gynoparae, males, or virginoparae between AgFS and AgFW at days 1, 6, 11, 16, and 21 are marked with ‘*’ (Student’s t-test, p < 0.05).
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Figure 4. Percentage of different A. glycines morphs induced in the F2 when the F1 of AgFS and AgFW was exposed to different photoperiods and 17 °C. (a) Gynoparae percentage of AgFS and AgFW at an 8L:16D-h photoperiod. (b) Gynoparae percentage of AgFS and AgFW at a 12L:12D-h photoperiod. (c) Gynoparae percentage of AgFS and AgFW at a 16L:8D-h photoperiod. (d) Male percentage of AgFS and AgFW at an 8L:16D-h photoperiod. (e) Male percentage of AgFS and AgFW at a 12L:12D-h photoperiod. (f) Male percentage of AgFS and AgFW at a 16L:8D-h photoperiod. (g) Virginoparae percentage of AgFS and AgFW at an 8L:16D-h photoperiod. (h) Virginoparae percentage of AgFS and AgFW at a 12L:12D-h photoperiod. (i) Virginoparae percentage of AgFS and AgFW at a 16L:8D-h photoperiod. The data are shown as the mean ± SE. The differences in percentage of gynoparae, males, or virginoparae between AgFS and AgFW are marked with ‘*’ (Student’s t-test, p < 0.05).
Figure 4. Percentage of different A. glycines morphs induced in the F2 when the F1 of AgFS and AgFW was exposed to different photoperiods and 17 °C. (a) Gynoparae percentage of AgFS and AgFW at an 8L:16D-h photoperiod. (b) Gynoparae percentage of AgFS and AgFW at a 12L:12D-h photoperiod. (c) Gynoparae percentage of AgFS and AgFW at a 16L:8D-h photoperiod. (d) Male percentage of AgFS and AgFW at an 8L:16D-h photoperiod. (e) Male percentage of AgFS and AgFW at a 12L:12D-h photoperiod. (f) Male percentage of AgFS and AgFW at a 16L:8D-h photoperiod. (g) Virginoparae percentage of AgFS and AgFW at an 8L:16D-h photoperiod. (h) Virginoparae percentage of AgFS and AgFW at a 12L:12D-h photoperiod. (i) Virginoparae percentage of AgFS and AgFW at a 16L:8D-h photoperiod. The data are shown as the mean ± SE. The differences in percentage of gynoparae, males, or virginoparae between AgFS and AgFW are marked with ‘*’ (Student’s t-test, p < 0.05).
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Table 1. Nymph stage duration and adult lifespan of AgFS on wild soybean and AgFW on soybean.
Table 1. Nymph stage duration and adult lifespan of AgFS on wild soybean and AgFW on soybean.
Temperature
(°C)		Nymph Stage Duration
(Day)		Adult Lifespan
(Day)
AgFS Fed
on Wild Soybean		AgFW Fed
on Soybean		AgFS Fed
on Wild Soybean		AgFW Fed
on Soybean
1710.06 ± 0.09 a11.20 ± 0.11 a *28.22 ± 1.93 ab38.70 ± 2.18 a *
207.06 ± 0.10 b8.15 ± 0.11 b *30.47 ± 1.72 a39.85 ± 1.46 a *
236.57 ± 0.12 c6.24 ± 0.09 c *24.63 ± 1.68 b24.18 ± 0.99 b
265.54 ± 0.09 d6.12 ± 0.14 c *20.50 ± 1.27 c23.78 ± 0.79 b *
294.60 ± 0.09 e5.22 ± 0.09 d *8.51 ± 1.03 d16.38 ± 0.83 c *
325.24 ± 0.11 f5.11 ± 0.07 d 9.10 ± 0.87 d10.81 ± 0.60 d
Note: Data are shown as mean ± SE. The differences in nymph stage duration or adult lifespan of each population among different temperatures are marked with a lowercase letter behind the mean ± SE. The differences in nymph stage duration and adult lifespan between AgFS and AgFW at each temperature are marked with ‘*’ (paired bootstrap test, p < 0.05).
Table 2. Adult fecundity and intrinsic rate of increase of AgFS on wild soybean and AgFW on soybean.
Table 2. Adult fecundity and intrinsic rate of increase of AgFS on wild soybean and AgFW on soybean.
Temperature
(°C)		Adult Fecundity
(Offspring/Female)		Intrinsic Rate of Increase
(Day−1)
AgFS Fed
on Wild Soybean		AgFW Fed
on Soybean		AgFS Fed
on Wild Soybean		AgFW Fed
on Soybean
1742.30 ± 2.10 c44.20 ± 2.02 b0.2321 ± 0.0024 c0.1989 ± 0.0019 d *
2051.32 ± 2.01 a45.28 ± 1.18 b *0.3236 ± 0.0059 b0.2772 ± 0.0047 c *
2344.80 ± 2.18 bc45.12 ± 1.77 ab0.3375 ± 0.0078 b0.3592 ± 0.0049 b *
2648.06 ± 1.91 ab49.22 ± 1.42 a0.4182 ± 0.0066 a0.3743 ± 0.0071 ab *
2914.96 ± 1.56 d32.22 ± 1.99 c *0.3459 ± 0.0126 b0.3884 ± 0.0099 a *
326.12 ± 0.62 e9.08 ± 0.80 d *0.1983 ± 0.0150 d0.2579 ± 0.0165 c *
Note: Data are shown as mean ± SE. The differences in adult fecundity or intrinsic rate of increase of each population among different temperatures are marked with a lowercase letter behind the mean ± SE. The differences in adult fecundity or intrinsic rate of increase between AgFS and AgFW at each temperature are marked with ‘*’ (paired bootstrap test, p < 0.05).
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Gao, B.; Yang, K.; Tian, Y.; Bai, B.; Tian, Z.; Liu, J. Adaptability of the Soybean Aphid Aphis glycines (Hemiptera: Aphididae) to Temperature and Photoperiod in a Laboratory Experiment. Insects 2024, 15, 816. https://doi.org/10.3390/insects15100816

AMA Style

Gao B, Yang K, Tian Y, Bai B, Tian Z, Liu J. Adaptability of the Soybean Aphid Aphis glycines (Hemiptera: Aphididae) to Temperature and Photoperiod in a Laboratory Experiment. Insects. 2024; 15(10):816. https://doi.org/10.3390/insects15100816

Chicago/Turabian Style

Gao, Bo, Kaice Yang, Yifan Tian, Bing Bai, Zhenqi Tian, and Jian Liu. 2024. "Adaptability of the Soybean Aphid Aphis glycines (Hemiptera: Aphididae) to Temperature and Photoperiod in a Laboratory Experiment" Insects 15, no. 10: 816. https://doi.org/10.3390/insects15100816

APA Style

Gao, B., Yang, K., Tian, Y., Bai, B., Tian, Z., & Liu, J. (2024). Adaptability of the Soybean Aphid Aphis glycines (Hemiptera: Aphididae) to Temperature and Photoperiod in a Laboratory Experiment. Insects, 15(10), 816. https://doi.org/10.3390/insects15100816

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