An Analysis of Female Postcopulatory Behavior in Drosophila suzukii and Drosophila biarmipes

Abstract

The fruit fly, Drosophila suzukii, is an invasive species that causes widespread crop damage in the United States. We examined a series of basic reproductive behaviors in this species in order to expand our knowledge of the life history of D. suzukii. We also conducted a comparison study using its sister species, D. biarmipes, to determine if the two species shared any similarities in sexual behavior. The behaviors investigated were sexual attractiveness, sexual receptivity, and offspring production. The sexual attractiveness and remating frequency (possibly reflecting sexual receptivity) of both D. suzukii and D. biarmipes females decreased significantly after an initial copulation and did not recover within 14 days. D. suzukii and D. biarmipes females also produced an average of 85.19 ± 6.27 and 104.45 ± 6.90 viable offspring, respectively, over the two weeks following the initial copulation, suggesting that they were able to store sperm over an extended period of time. We also found that the sexual attractiveness of virgin D. suzukii decreased as they aged. This decline may be related to nutrition, as their attractiveness did not diminish when the females were raised on a blueberry as well as standard media and yeast. Our results, coupled with the findings of other studies investigating basic life history and reproductive biology parameters, can aid in the effort to halt the spread of D. suzukii by informing and refining future and current pest management strategies.

Introduction

The spotted wing fruit fly, Drosophila suzukii, is a well-known invasive fruit pest in Europe and the United States, targeting thin-skinned fruits such as blueberries, raspberries, cherries, and grapes (Lee et al. 2011; Walsh et al. 2011; Asplen et al. 2015). The species originated in Southeast Asia, and has since spread across the globe, reaching the American mainland in the late 2000s (Goodhue et al. 2011). Females lay their eggs in ripe, live fruit using a serrated ovipositor, making them a particular nuisance for agriculture. This is in stark contrast to most Drosophila, which lay their eggs in fallen, rotting fruit (Bellamy et al. 2013; Kinjo et al. 2013; Steffan et al. 2013).

The commercial impact of D. suzukii has been extensive, with estimated crop losses of 20–50%, and the potential for upwards of $500 million in lost annual revenue (Bolda et al. 2010; Walsh et al. 2011; Cini et al. 2012). Given this substantial economic burden, considerable research has gone into the development of effective eradication and management techniques to combat future crop loss (Beers et al. 2011; Cini et al. 2012). Scientists have determined that softer fruits, like blueberries, raspberries, blackberries, and strawberries are the crops most at risk for infestation by D. suzukii, and that given the choice, females will oviposit in these fruits compared to fruits with slightly firmer skin, like grapes and cranberries (Lee et al. 2011; Bellamy et al. 2013; Burrack et al. 2013; Kinjo et al. 2013; Steffan et al. 2013). With regard to pest control, studies have shown that commercially available predators, as well as entomopathogenic fungi and nematodes, have limited ability to suppress D. suzukii infestations (Woltz et al. 2014), although there is some indication that several hymenopteran parasitoids species have had moderate success (Daane et al. 2016; Knoll et al. 2017).

Despite the attention given to D. suzukii, it is important to note that most studies have focused on applied research, particularly pest management and eradication strategies. Relatively little is known about the life history and behavior of D. suzukii, especially when compared to other fruit flies such as the lab staple D. melanogaster (Bastock and Manning 1995; Greenspan and Ferveur 2000; Prasad and Joshi 2003). The sexual and reproductive behavior of D. suzukii should be considered part of an integrated program of pest management as these aspects of their biology have obvious implications on the development of pest control methods. Knowing when, how, and how frequently the flies court, mate, and oviposit could help refine current management methods by identifying ideal times for the application of pesticides, improving population models that guide pest control strategies, and elucidating environmental factors that impact sexual maturation, mating, and offspring production.

In many insect species, females undergo a series of behavioral changes following copulation (Gillot 2003). Egg production and oviposition rates increase (Wolfner 2002; Chapman et al. 2003), while sexual attractiveness and receptivity decrease (Chapman et al. 2003; Kubli 2003). Females become less attractive to males, less willing to remate, and, if remating does occur, the duration of copulation may be different than that seen with virgin females (Singh and Singh 2004). These changes have been observed in drosophilids such as D. melanogaster, D. ananassae, D. simulans, and many others, and the effects last for varying amounts of time (Manning 1962; Singh and Singh 2004). The biochemistry driving these behavioral changes is well understood, resulting from peptides found in seminal fluid, particularly those produced by the male accessory glands (ACPs) (Leahy and Lowe 1967; Wolfner 1997; Gillot 2003). The most well-known of these peptides is Acp70A, or the sex peptide (SP). SP impacts both egg production and receptivity – virgin D. melanogaster females injected with purified SP become unreceptive for mating and increase their egg production for a period of 1–2 days post-injection (Manning 1962; Chapman et al. 2003).

D. suzukii is known to produce a peptide homologous to SP in D. melanogaster (Schmidt et al. 1993). This peptide may induce similar postcopulatory behaviors in females, though studies exploring these changes have yet to be completed for D. suzukii. Postmating behavior, however, has been investigated in D. biarmipes, another spotted-wing drosophilid that originated from Southeast Asia and the most closely related (sister) species to D. suzukii (McRobert et al. 1997; Yang et al. 2012; Ometto et al. 2013). The sexual attractiveness of mated D. biarmipes females has been shown to decline immediately after mating and does not recover to premating levels over a period of two weeks following initial copulation (McRobert et al. 1997). Since these two species are close taxonomic relatives, and D. suzukii males are known to possess the sex peptide homologue, it is reasonable to suggest that D. suzukii females also undergo a similar series of postcopulatory changes. In this study, we analyze and quantify what happens to both D. suzukii and D. biarmipes females after they copulate, including any modifications in sexual attractiveness, sexual receptivity, and offspring production.

Materials & Methods

Stocks

The D. suzukii stocks were derived from flies collected in the wild in Philadelphia, PA in August, 2015. The D. biarmipes stocks, derived from a natural population in Cambodia, were obtained from The National Drosophila Species Stock Center in the Fall of 2015. Both stocks were maintained in mass culture on a diet of Carolina Instant Drosophila Media (Formula 4–24), with yeast. The media was hydrated with a solution of 0.5% propionic acid to inhibit the potential for mold growth. A moistened paper towel was placed into each stock bottle to provide more space for pupation. The D. suzukii stock bottles were supplemented with frozen blueberries that had been thawed. All stocks were maintained in an incubator at a constant temperature of 25 °C on a 12:12 LD cycle. Studies utilizing these stocks were initiated in February, 2016.

Virgin flies were collected under CO2 anesthesia within six hours of eclosion. Females were stored in groups of 5–10 (unless otherwise noted), while males were stored individually, in vials containing medium, yeast, and a moistened paper towel.

Behavioral Assays

Behavioral assays were performed between 0800 and 1200 at 25 ± 2.5 °C. Virgin males and females were 3–5 days old when tested unless otherwise noted. All tests were done in real time and observed with the naked eye.

Courtship Assays

The goal of these assays was to understand how long females remained unattractive to potential mates after a copulation event. A single male-female pair was aspirated without anesthesia into a cylindrical plastic observation chamber (volume, ca 0.2 cm3) and observed for 500 s. During this time, the courtship index (CI), or the percentage of time the male performed any courtship behavior towards the female, was calculated. The CI for twenty virgin pairs was recorded for both D. suzukii and D. biarmipes. To control for the effect of age on female attractiveness, an additional set of tests were run with new females that were 10–12 days old, (N = 20 for both D. suzukii and D. biarmipes). This time-point was chosen as mated females in the 7-day post-mating trials were a total of 10–12 days old (they were originally mated at 3–5 days old). For D. suzukii only, an extra series of tests were conducted in which the virgin females were raised on Drosophila media, yeast, and a thawed blueberry. The blueberry was punctured to allow access to the fruit. Twenty virgin females raised on these conditions were tested when they were 3–5 days old, and another twenty were tested when they were 10–12 days old.

Twenty mated females of each species were also kept and tested 1-h, 1-day, and 7-days after initial copulation (a new set of 20 females for each time point) to determine when sexual attractiveness recovered. The mated females were produced by aspirating a virgin female into a vial (with hydrated Instant Dros. Media & yeast) with a virgin male. The vial was observed for two hours, or until copulation was successfully completed. We selected two hours as our observation interval as previous studies have shown that most copulation occurs within the first 30 min of a pairing, so two hours provided sufficient time for copulation to occur (Redavi et al. 2015). The female was then removed by aspiration and stored individually in a fresh vial with medium and yeast until the next trial (D. suzukii females were given a thawed blueberry as well).

Copulation Assays

The goal of these assays was to understand how long females remained unreceptive to potential mates after an initial copulation event. A single male-female pair was aspirated, without anesthesia, into vials with media & yeast. These vials were laid on their sides and observed for 60 min, or until the pair successfully copulated. During this time, the copulation frequency (fraction of total females that mated within the observation period), copulation latency (time from placement in the vial until copulation commenced), and copulation duration were recorded (N = 20 for 3–5 day old virgin D. suzukii females, N = 20 for 3–5 day old virgin D. biarmipes females).

To determine the proportion of females that remated, mated females were aspirated, without anesthesia, into vials containing media and yeast, and a virgin male and observed for 60 min. Copulation frequency, copulation latency, and copulation duration were recorded. Mated females were tested 1-day post-copulation, 7-days post-copulation, and 14-days post-copulation (N = 20 in each assay for D. suzukii, N = 20 for 1-day post-copulation D. biarmipes, N = 20 for 7-day post-copulation D. biarmipes, N = 12 for 14-day post-copulation D. biarmipes). Each female was used in only one post-copulation test. The mated females were produced and maintained in the same manner as the mated females for the courtship assays.

Offspring Production

Twenty mated females of each species were kept in numbered vials for 7 days after an initial copulation, with medium, yeast, and a wetted paper towel (D. suzukii females were also provided with a thawed blueberry). After 7 days, they were transferred to a new numbered vial, and kept for an additional 7 days. At the end of the 2 weeks, the females were removed and incorporated in the copulation assays (for the 14-day time point). Larvae and pupae were counted 3–5 days after the female was removed from either the week 1 or week 2 vial, using a sucrose-medium submersion technique. In this technique, the medium was flushed from each vial with a 20% sucrose solution and stirred. This mixture caused the medium to sink to the bottom while larvae and pupae floated, allowing them to be counted (see Frank et al. 1995). Larvae and pupae attached to the paper towels as well as young adult offspring were also included in the total offspring count.

Statistical Analysis

Courtship assays (CI at each time point) were analyzed using a one-way ANOVA with “female status” (i.e. virgin, 1-h post-copulation, 24-h post-copulation, etc.) as the fixed factor. Each species was analyzed independently of the other. All courtship indices were arc-sine transformed to ensure a normal distribution. For the copulation assays, the mean courtship latency and mean courtship duration for virgin pairs was compared between species with an unpaired t-test assuming unequal sample variances. Remating frequency was analyzed using either a chi-squared test of homogeneity or a Fisher’s exact probability test at each time point (1-day post-copulation, 7-days, and 14-days) across species, and across time points within species. For the offspring production assays, the mean number of offspring produced each week was compared between species with a t-test assuming unequal variances. All analyses were performed in R v.3.6.1 (R Core Team 2019).

Results

In both species, 3–5 day-old virgin females were more attractive than females that had copulated 1-h, 1-day and 7-days prior (Figs. 1 and 2). For D. biarmipes females, there was no significant difference in sexual attractiveness between 3 and 5 day-old virgins and 10–12 day-old virgins (One-Way ANOVA & Tukey’s Test, df = 99, F = 11.19, p = 1.00) (Fig. 1). In comparison, 3–5 day-old virgin D. suzukii females were significantly more attractive than their 10–12 day-old counterparts (One-way ANOVA & Tukey’s Test, df = 139, F = 4.49, p = 0.011) (Fig. 2). There was also no significant difference in attractiveness between 10 and 12 day-old virgin D. suzukii females and females that had copulated 7-days prior (p = 1.00) (Fig. 2). However, when D. suzukii females were raised with a blueberry, in addition to the standard diet of media and yeast, the difference between 3 and 5 day-old virgins and 10–12 day old virgin females disappeared (Fig. 2). These 10–12 day-old virgin females raised on blueberries were more attractive than females 7-days post-copulation as well (Fig. 2).

Fig. 1
figure1

Sexual attractiveness of D. biarmipes females measured as mean CI (± SE) of D. biarmipes males in response to mated females 1 h., 1 day, and 7 days post initial copulation, and virgin females that were 3–5 days old (0 h.) and 10–12 days old (7 days). Error bars represent standard error

Fig. 2
figure2

Sexual attractiveness of D. suzukii females measured as mean CI (± SE) of D. suzukii males in response to and mated females 1 h., 1 day, and 7 days post initial copulation, virgin females that were 3–5 days old (0 h.) and 10–12 days old (7 days), and virgin females raised on a blueberry (in addition to standard media and yeast). Error bars represent standard error

Virgin D. biarmipes pairs had a shorter (but not significantly different) copulation latency compared to virgin D. suzukii pairs (t-test assuming unequal sample variances, df = 14.56, t = −1.70, p = 0.11) (Fig. 3). There was also no difference in the copulation duration of virgin D. biarmipes and virgin D. suzukii pairs (t-test assuming unequal sample variances, df = 11.54, t = −1.16, p = 0.27) (Fig. 3). Significantly more virgin D. biarmipes pairs copulated compared to virgin D. suzukii pairs (χ2 = 10.8, df = 1, p = 0.001). However, there was no difference in the number of pairs that remated for either species at any of the time points tested (1-day post-copulation, 7-days, or 14-days) (1-day post-cop: χ2 = 0.28, df = 1, p = 0.60; 7-days post-cop: Fisher’s exact test, p = 1.00; 14-days post-cop: Fisher’s exact test, p = 1.00). When comparing mating frequency within D. biarmipes, significantly more virgin females mated than did females 1, 7 or 14 days post-mating (χ2 = 52.51, df = 3, p = 2.33 × 10−11). D. suzukii females experienced a similar decline in mating frequency post-copulation as well (χ2 = 11.76, df = 3, p = 0.008). The percentage of females mating dropped from 100 and 50% (D. biarmipes and D. suzukii, respectively) to less than 16% for both species at any of the time points.

Fig. 3
figure3

Mean copulation duration (± SE) and mean copulation latency (± SE) of D. suzukii & D. biarmipes virgin pairs. Error bars represent standard error

D. biarmipes females produced more offspring during the first and second week post-copulation (52.38 ± 3.55 and 49.81 ± 5.55 offspring, respectively) compared to D. suzukii females (36.32 ± 3.23 and 47.19 ± 4.67, respectively). Only the difference between species in the first week was significant, however (t-test assuming unequal sample variances, Week 1: df = 43.90, t = 3.34, p = 0.002, Week 2: df = 34.97, t = 0.36, p = 0.72). Over the entire 14-day period following copulation, D. biarmipes females (104.45 ± 6.90 offspring) produced significantly more viable offspring than D. suzukii females (85.19 ± 6.27 offspring) (t-test assuming unequal sample variances, df = 33.98, t = 2.07, p = 0.046).

Discussion

Drosophila suzukii and Drosophila biarmipes share many similarities in behavior and morphology, as is often the case with sister species. Both are small, “spotted-wing drosophila,” with the males exhibiting dark pigmentation on the outer edge of their wings (Kopp and True 2002). The courtship displays of D. suzukii and D. biarmipes are remarkably alike, and include orientation, tapping, full extension of both wings, licking, and attempted copulation (Redavi et al. 2015; personal observations). Despite their many likenesses, however, there are major differences in the reproductive behaviors of these two species. For example, D. biarmipes males copulate and court more vigorously than D. suzukii males (personal observations) and D. suzukii females oviposit in fresh fruit, instead of the rotten or overripe fruit used by D. biarmipes and many other drosophilids (Bellamy et al. 2013; Kinjo et al. 2013; Steffan et al. 2013). Our goal was to further identify similarities and differences between these two species, particularly as it pertains to postcopulatory behaviors.

The sexual attractiveness and remating frequency (possibly reflecting sexual receptivity) of females from both species significantly decreased immediately after an initial copulation and did not recover up to 14 days later. It is possible that these behavioral changes are affected by compounds (like the sex peptide) that are transmitted from males to females during copulation (Chapman et al. 2003). While SP in D. suzukii and D. biarmipes has not been closely investigated, it is known to play a prominent role in eliciting post-copulatory behavioral changes in D. melanogaster, including a sharp decrease in sexual receptivity and attractiveness for approximately five days post-copulation (Chapman et al. 2003). We have also demonstrated the ability of D. suzukii and D. biarmipes females to store and utilize sperm for more than 7 days post-copulation, which may be associated with their prolonged decrease in attractiveness and receptivity. In the future, we hope to extend these attractiveness and receptivity assays over a longer time period following an initial mating, to determine whether they ever return to virgin-like levels. Similarly, it would also be of interest to investigate if remating shortens the life span of these females, as has been suggested in other drosophilids (Fowler and Partridge 1989).

During the process of characterizing the postcopulatory behavior of D. suzukii and D. biarmipes, we uncovered major differences in the sexual behavior of these two species. First, as previously noted, D. biarmipes males appeared to court more vigorously and more successfully than D. suzukii males. A significantly greater proportion of virgin D. biarmipes pairs copulated compared to virgin D. suzukii pairs, and they did so in a shorter amount of time. This may simply be an artifact of captive rearing and testing however, as the scope and range of D. suzukii infestations worldwide suggest that they are a highly productive species in the wild. Second, we saw that while the sexual attractiveness of D. biarmipes virgin females remained roughly constant, regardless of age, the sexual attractiveness of D. suzukii virgin females significantly decreased over time. This decrease was unexpected, as 10–12 days-old females are relatively young (the life expectancy of D. suzukii flies is greater than 60 days – Walsh et al. 2011) and should be sexually active (Kanzawa 1939). Sex appeal, therefore, should not decrease over this short period of time, and does not in many other drosophilids including D. melanogaster and D. biarmipes (McRobert et al. 1997). This suggests that our D. suzukii females were missing something crucial during stock maintenance and may not have been getting proper nutrition. Potential mates may detect this malnourishment (possibly via olfactory cues) and be less likely to court, thus lowering sexual attractiveness and receptivity.

To address the potential effects of malnourishment under laboratory conditions, we provided virgin D. suzukii females with punctured blueberries, mimicking the availability of fallen, overripe fruit found normally in an orchard. We found that the sexual attractiveness of the 10–12 days-old virgin females “recovered” when provided with the blueberry, and the effect of age on sexual attractiveness was eliminated. These findings suggest that the blueberries are not important just for oviposition, as was previously thought, but also for proper nutrition of the adult female. It is important to note that this dependency on blueberries could be because the berries also provide some sort of olfactory cue or signal important for reproductive behavior as well. Several studies on tephritid fruit flies have shown that plant-based chemical compounds may influence male mating success, female attractiveness, and the propensity of a female to remate (see Segura et al. 2018 for a review). Our results suggest a similar phenomenon may occur in D. suzukii, and that the very fruit females feed on and oviposit in may also play a pivotal role in their reproductive success, either directly or indirectly. Further studies detailing the specific effects of proper nutrition and exposure to fruit compounds on D. suzukii mating behavior are needed, particularly as these results could inform future pest management strategies.

Innate differences in the mating ability of males, or the “choosiness” of females, may also impact our results, in addition to the influence of proper nutrition or chemical cues on reproductive behavior. Mate choice has been investigated in several fruit fly species over the past few decades. Singh and Chatterjee (1987) demonstrated that D. biarmipes females preferentially mated with males that possessed larger apical black wing patches, while Talyn and Dowse (2004) revealed that D. melanogaster males with higher quality courtship songs mated most frequently. As D. suzukii males also use both visual and auditory and cues during courtship, it is likely that a similarly dynamic sexual selection process occurs in D. suzukii as well. If true, it is possible our results may have been influenced by the outcome of outsized pairings between highly discriminant females and less successful males, or vice versa. While our sample sizes and sampling scheme should be robust enough to overcome such effects, further research into mate choice and sexual selection in D. suzukii and D. biarmipes is warranted.

Postcopulatory behavior is an important characteristic of life history in Drosophilids, and has been examined in a number of species, including D. melanogaster (Cook and Cook 1975), D. ananassae (Singh and Singh 1999; Singh and Singh 2001; Singh and Singh 2001a, b; Singh and Singh 2004), and members of the D. bipectinata species complex (Singh and Singh 2013). Here, we have helped to expand the knowledge of such behaviors in drosophilids by examining the invasive pest species, D. suzukii, along with its sister species, D. biarmipes, which does not act as a pest. However, this study goes beyond simply adding to our understanding of the basic reproductive biology of these species. Our results, and others like them, are also crucial in informing pest control and eradication tactics.

Characterizing the mating behaviors of agricultural pests like D. suzukii can aid in the development and refinement of integrated pest management methods by identifying when, how, how frequently and under what environmental conditions the flies court, mate, and oviposit. For example, our findings may offer added hope for the effectiveness of the Sterile Insect Technique (SIT), a strategy in which sterile males, released into the wild, mate with virgin wild females who then lay unfertilized eggs (Lanouette et al. 2017). We demonstrated that D. suzukii females, once mated to sterile males, could display a marked reduction in remating frequency with wild fertile males, and an overall decrease in fertilized egg production. Similarly, our results on the impact of proper nutrition on the reproductive behavior of D. suzukii could be coupled with previous studies on the influence of dietary microbes and nutrient-dependent microbiota (Bellutti et al. 2018; Bing et al. 2018) on larval development to inform innovative behavioral control strategies. Further work on the basic life history and reproductive biology of D. suzukii and related species will only continue to aid in the refinement and design of future pest management techniques.

Data Availability

Not applicable.

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All authors conceived and planned the experiments. R.D.C. and M.D. carried out the experiments and analyzed the data, with supervision from J.T.F and S.P.M. R.D.C., J.T.F. and S.P.M. wrote the manuscript.

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Correspondence to René D. Clark.

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Clark, R.D., DiPiero, M., Fingerut, J.T. et al. An Analysis of Female Postcopulatory Behavior in Drosophila suzukii and Drosophila biarmipes. J Insect Behav 33, 193–200 (2020). https://doi.org/10.1007/s10905-020-09761-x

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Keywords

  • Drosophila suzukii
  • Drosophila biarmipes
  • postcopulatory behavior
  • pest