TY - JOUR
AU - Long, Tristan A, F
AB - Abstract Individuals are faced with decisions throughout their lifetimes, and the choices they make often have important consequences toward their fitness. Being able to discern which available option is best to pursue often incurs sampling costs, which may be largely avoided by copying the behavior and decisions of others. Although social learning and copying behaviors are widespread, much remains unknown about how effective and adaptive copying behavior is, as well as the factors that underlie its expression. Recently, it has been suggested that since female fruit flies (Drosophila melanogaster) appear to rely heavily on public information when selecting oviposition sites, they are a promising model system for researching patch-choice copying, and more generally, the mechanisms that control decision making. Here, we set out to determine how well female distinguish between socially produced cues, and whether females are using “relevant” signals when choosing an oviposition site. We found that females showed a strong preference for ovipositing on media patches that had been previously occupied by ovipositing females of the same species and diet over other female outgroups. However, in a separate assay, we observed that females favored ovipositing on media patches that previously housed virgin males over those exhibiting alternative conspecific signals. Our results confirm that females use cues left behind by other flies when choosing between potential oviposition sites, though their prioritization of these signals raises serious questions as to whether fruit flies are employing copying behavior, or are instead responding to signals that may not be of relevance to oviposition site suitability. Introduction An individual’s fitness is often impacted by the choices it makes throughout its lifetime, be it regarding its habitat use, dietary decisions, the nature of its social interactions (including mate choice), and/or where its offspring are to be reared, and consequently individuals are often under strong selection to make optimal choices. An important part of the decision-making process is obtaining relevant information through sampling of the environment in order to reduce the uncertainty associated with alternate potential behavioral outcomes (Danchin et al. 2004; Dall et al. 2005; Valone 2007). To achieve this, individuals must be able to perceive and interpret a variety of different signals in their environment, weigh their options, and possibly commit them to memory (Drugowitsch et al. 2012). This is a potentially expensive endeavor in terms of time and energy, and individuals may attempt to avoid these costs by copying the behaviors and decisions expressed by others in their environment, using this “public” information in lieu of their own “private” cost-benefit information and assessment (Valone 1989; Battesti et al. 2012). Socially acquired information may take the form of evolved “signals,” used to communicate between individuals and/or “inadvertent social information” which is generated as a side effect of the actions performed by others (Danchin et al. 2004; Dall et al. 2005). While public information may come from conspecifics, it can also be produced by other species (reviewed in Avarguès-Weber et al. 2013). Copying behavior is seen in a wide range of species in many decision-making contexts, including determining suitable habitat or foraging sites, choosing a mate, and/or when deciding where to oviposit eggs and rear offspring (reviewed in Heyes and Galef 1996; Valone and Templeton 2002; Galef and Laland 2005; Wertheim et al. 2005; Valone 2007; Grüter and Leadbeater 2014). Consequently, understanding how, when, and why individuals use public information is important to understanding the mechanisms underlying decision-making processes, and their influence on the process of biological evolution (Leadbeater 2009; Grüter and Leadbeater 2014; Depetris-Chauvin et al. 2015). Due to the widespread usage of public information by numerous taxa in many decision-making contexts, and the apparent low costs of acquiring this information, it is commonly assumed that social learning is inherently adaptive (Laland 2004). While copying may be adaptive in many situations (Galef 1995), the potential downside of valuing public over private information comes from trusting that one’s conspecifics have themselves made suitable decisions, and that their cues are a reliable source of information, which may not always be the case (Giraldeau et al. 2002; Laland 2004; Kendal et al. 2009; Hoppitt and Laland 2013). For example, in Norway rats (Rattus norvegicus), food preferences can be altered by experimentally exposing individuals to a conspecific who has been fed a different, novel (but equally palatable) food by letting them smell the scent on their breath (Galef and Wigmore 1983). This change in preference can persist for weeks and is not seen when rats are exposed to the novel food alone (Galef 1989). While this copying may be adaptive by promoting the use of new food sources, by overwriting an individual’s prior food preferences, acquired though personal experiences, it may instead prove costly if those preferences were actually beneficial (Galef 1989), and could lead individuals to consume food that they would have otherwise avoided (Galef 1985). Similarly, while guppies (Poecilia reticulate) may benefit from using information obtained from conspecifics when deciding which (of two equivalent) routes to follow to get to a foraging site (Laland and Williams 1997), by relying heavily on public information they may make maladaptive choices by following a longer (and more energetically costly) route if this is the path taken by the demonstrator conspecifics (Laland and Williams 1998). Theoretical models have also suggested that universal and indiscriminate copying is not an adaptive strategy, and will only enhance individual fitness if most individuals in the population are asocial learners who generate accurate information about their environment (Boyd and Richerson 1985; Giraldeau et al. 2002). However, social learning can be adaptive if individuals are selective about when they use public information, and about which specific individuals they copy (Laland 2004; Kendal et al. 2009; Hoppitt and Laland 2013). Furthermore, different individuals may use social information to different extents depending on their own genotype, developmental stage/age, physiological state, and/or prior experiences (Bell 1990; Foucaud et al. 2013; Depetris-Chauvin et al. 2015). The adaptive use of social information may also depend on environmental heterogeneity, as the value of the public information to the observer depends on the degree to which the demonstrator provides reliable and relevant information, which not be the case if the two parties experience different environments (Boyd and Richerson 1985; Boyd and Richerson 1988). Thus, when considering social information use and its adaptive value, it is important to consider the qualities the demonstrators, the observers, as well as the environment context in which copying behavior may be occurring. The use of social cues by female fruit flies (Drosophila melanogaster) to inform their oviposition decision-making process was first reported in the 1960’s (see del Solar and Palomino 1966; Mainardi 1968; Ayala and Ayala 1969; Mainardi 1969) but this phenomena has recently received considerable attention from a new generation of behavioral ecologists and geneticists (e.g., Wertheim, Dicke, et al. 2002; Wertheim, Marchais, et al. 2002; Sarin and Dukas 2009; Battesti et al. 2012; Golden and Dukas 2014; Lin et al. 2015; Duménil et al. 2016). In fruit flies, there may be several potential advantages to copying oviposition site choices (Durisko et al. 2014) as laying one’s eggs in proximity to those of conspecifics may allow the offspring to take advantage of sites of higher nutritional value (Duménil et al. 2016), enhanced microbial activity (Gilbert 1980; Wertheim, Dicke, et al. 2002; Wertheim, Marchais, et al. 2002), and/or communal foraging (Dombrovski et al. 2017). Oviposition site choice by female D. melanogaster appears to be heavily influenced by the behavior of conspecifics as an individual’s likelihood of ovipositing on a specific media type is increased if they have previously encountered a demonstrator female ovipositing on media of the same type (Sarin and Dukas 2009; Battesti et al. 2012). Drosophila melanogaster’s use of public information when ovipositing does not even require the direct physical observation of conspecifics. Duménil et al. (2016) found that mated females were more likely to lay eggs on media that had previously been exposed to either mated female or mated male demonstrators, compared to unexposed media. Follow-up assays indicted that mated females preferred ovipositing onto media that had been exposed to other mated females over media that had been previously exposed to either virgin males, mated males, or virgin female demonstrators. The great importance of public information to D. melanogaster was also seen by Golden and Dukas (2014) who examined how flies much used a reference media (which had not been exposed to larvae and was of high nutritional quality), compared to an experimental media patch of varying nutritional quality that had been endowed with public information in the form of larval exposure. They observed that females exhibited a strong bias toward ovipositing on media that contained larvae, even if it only contained a third of the nutrition available of the reference media (and ultimately lacked sufficient resources to ensure any offspring survival). A subsequent assay in which larvae were physically removed from the social plates (to avoid potential confounds associated with visual cues from larval presence and the effect of competition against the focal offspring), yielded similar results, suggesting that ovipositing females used gustatory/scent cues (presumably biochemical cues left behind by conspecifics females) when copying (Golden and Dukas 2014). This hypothesis was supported by a parallel study that found that both larvae and adult flies were less likely to visit axenic (bacteria-free) media than either media that had been exposed to larvae with intact microbiomes or from axenic media supplemented with bacterial odors (Venu et al. 2014). Similarly, Duménil et al. (2016) found that allowing a demonstrator mated female to associate with media devoid of yeast (a valuable resource to adult and larval flies alike), made that media patch equally preferable to a later ovipositing females as a patch of unexposed media that actually contained yeast. Together, these studies suggesting that ovipositon-site copying by females flies involves cues (i.e., pheromones, such as cis-vaccenyl acetate, cVA (Bartelt et al. 1985), cuticular hydrocarbons, CHCs, and/or microbiotic cues) left behind by demonstrators. The overall implication of these studies is that D. melanogaster strongly prioritizes public information over private information when deciding where to oviposit, to such an extent that they will miss out on large and meaningful differences in media nutritional quality that are potentially relevant to their lifetime fitness. Based on these findings, Golden and Dukas (2014) suggested that D. melanogaster would serve as a useful model for understanding the factors that shape patch-choice copying and more generally about adaptive social information use. There are numerous tools available in D. melanogaster that can be used to study the genetic and neural basis for variation in decision making (e.g., Yang et al. 2008; Miller et al. 2011) and in this species public information is also used when learning spatial learning tasks (e.g., Foucaud et al. 2013) and by females when choosing mates (e.g., Loyau et al. 2012; Mery et al. 2009; Dagaeff et al. 2016; Monier et al. 2018). While the behavior of individuals may differ between the lab and in the field (e.g., Markow 1988; Zala et al. 2012), the use of laboratory stocks of D. melanogaster permits controlled, manipulative, experimental studies of social information usage and may provide insights into the molecular basis for these behaviors that might not otherwise be possible (Leadbeater 2009; Grueter and Leadbeater 2014). Thus studying the factors that influence public information use in making oviposition site decisions in D. melanogaster may lead to a broader understanding of the evolution of social learning and its adaptive potential. Our research was largely inspired by the studies of Golden and Dukas (2014) and Duménil et al.’s (2016) who found that female D. melanoagaster are able to detect and interpret cues left behind by demonstrator conspecifics. However, these signals may vary due to differences associated with the species, age, sex, mating status, social experience, and/or the environment the demonstrator developed in (Ferveur 2005; Everaerts et al. 2010; Chandler et al. 2011; Farine et al. 2012; Dekker et al. 2015; Han et al. 2017; Bing et al. 2018; Jehrke et al. 2018). Identifying relevant cues can be a challenge to potential observers, and their inability to do so may result in maladaptive choices (Depetris-Chauvin et al. 2015). As such, we set out to get a better understanding of the specificity and/or limitations of this copying behavior in D. melanogaster. We did this in two ways: 1) by examining how individual females responded to cues produced by a range of both conspecific and heterospecific Drosophila demonstrators; 2) by focusing on how female behavior varies in response to the cues left behind by D. melanogaster demonstrators that differ in their mating status and/or sex, and whether female copying behavior was similar for virgin and mated individuals. In our first experiment, we examined if mated females were selective in what public information they used. Since different species of Drosophila exhibit different oviposition habitat preferences (Barker 1971; Richmond and Gerking1979; Chess and Ringo 1985) presumably due to selection for their species-specific optimal larval developmental conditions (e.g., Matavelli et al. 2015; Young et al. 2018), the different cues produced by heterospecifics (see Ferveur et al. 2005; Symonds and Wertheim 2005; Chandler et al. 2011; Dekker et al. 2015) could yield information on the suitability of alternate potential oviposition sites. Furthermore, as pheromones, CHCs and microbiotic profiles of D. melanogaster conspecifics are influenced the specific environment in which they develop (Blum et al. 2013; Billeter and Wolfner 2018; Bing et al. 2018) this may provide an additional source of intraspecific public information. Laland (2004) argued that individuals should logically be more likely to copy individuals that are most similar to themselves, as such demonstrators have a greater probability of providing beneficial information to the copier. Thus, we hypothesized that female fruit flies would be more likely bias their public information use toward the cues produced by their most similar conspecifics. In our second experiment, we focused our attention on intraspecific social information usage. If patch-choice copying is based on the need to locate suitable oviposition sites, then the most logical source of relevant information for a mated female would presumably come from mated female demonstrators. As there is sexual dimorphism in mircobiomes, pheromones, and CHCs (Everaerts et al. 2010; Ferveur 2005; Simhadri et al. 2017), and that CHC profiles differ between mated and virgin individuals (Everaerts et al. 2010; Duménil et al. 2016), we hypothesized that mated females would preferentially choose oviposition sites that displayed cues produced by mated female demonstrators (as was seen by Duménil et al. 2016). We also investigated whether mated and virgin females used public information in the same way. Drosophila melanogaster females choose different types of food depending on their mating status (Ribeiro and Dickson 2010; Camus et al. 2018), presumably because of differences in their nutritional requirements as in mated females, egg production is often limited by access to live yeast in their diets (Drummond-Barbosa and Spradling 2001; Stewart et al. 2005). Thus, we hypothesized that copying behavior in females would differ depending on their mating status, with each type of female associating more with the cues originating from demonstrator females of the same mating status. Overall, the goal of these studies is to better characterize the nature of copying behavior in D. melanogaster and to gain better insight into the factors that influence their oviposition site decisions. MATERIALS AND METHODS Population protocols and fly maintenance All focal individuals used in our assays were D. melanogaster obtained from the “Ives” (hereafter “IV”) population: a large, outbred wild-type population that originated from a wild sample caught in Amherst MA, USA in 1975 (Rose 1984). We also used flies from 1) the IV-bwD population, which is genetically similar to the IV population, with the exception that a dominant brown-eyed allele (bwD) has been introgressed (via repeated backcrossing) into the IV genetic background; 2) a population of Drosophila suzukii (aka Spotted Wing Fruit Fly, SWD) which was established from individuals eclosing from raspberries that were collected in Cambridge ON, Canada; 3) Drosophila simulans from a population homozygous for a recessive, brown-eyed allele (bw1) that was originally obtained from the University of California San Diego Drosophila Stock Centre (Stock-ID: 14021-0251.064). Flies in all populations are reared in vials containing ~10 mL of a banana/agar/killed-yeast food (with a protein to carbohydrate ratio of ~1:3, Rose 1984) that we refer to as “standard media” and develop in an incubator at 25 °C and 60% humidity on a 12 L:12 D diurnal light cycle. All populations (with the exception of D. suzukii) develop at an initial density of approximately 100 eggs per vial and are cultured on a nonoverlapping 14-day cycle (Rose 1984; Martin and Long 2015) while the D. suzukii population is maintained on a 21-day culture cycle, and vials initially contain ~40 eggs each at the start of each culture cycle (see Young et al. (2018). Can females distinguish between intra- and interspecific cues for suitable oviposition sites? In our first major assay, we set out to determine how well female flies discriminated between (presumably) different cues left behind by a range of different drosophilids demonstrators. Focal flies were obtained by placing sets of IV eggs into vials containing media with a 24:1 ratio of protein to carbohydrates (using the recipe in Lihoreau, Poissonnier, et al. 2016; Young et al. 2018), and were collected as adult virgins (within 8 h of eclosion from pupae) ~3–4 days before the start of the assay (hereafter “IV-24” flies). The focal IV-24 females used in the assay were housed in vials in sets of 10 then combined with similarly aged IV-24 males for 24 h before the start of the assay. Males were then removed (under light CO2 anesthesia) 2 h prior to the start of the assay, and mated females were returned to their vials. To measure fly oviposition behavior, we placed mated focal females into “cafeteria-style” choice arenas (described in Young et al. 2018) consisting of inverted transparent plastic boxes (KIS Omni Box, 20.3 × 15.9 × 9.6 cm) which had been modified by adding mesh-covered vent holes along the boxes’ upper edges. At the bottom of each arena, we arranged five small petri dishes (lids from Kartell 733/4 polyethylene 20 mL sample vials) that each contained 1.5 mL of standard media. Four of the five dishes presented cues associated with different drosophilids demonstrators while the fifth had not been exposed to any flies and served as a control dish. Fly-cue dishes were created by exposing the dish’s media to groups of five mated demonstrator females overnight (~18 h) in an inverted Kartell 20 mL sample vial (which contained a foam-stoppered hole to permit air flow). All demonstrator females were the same age (posteclosion) as the focal females, and had been housed with similarly aged males for ~24 h to being placed into the sample vials. The four fly-cue dish treatments were as follows: IV-24 females mated to IV-bwD males (these dishes were hypothesized to present the most similar cues to the focal IV-24 flies, and would thus presumably provide the most meaningful information about oviposition site suitability); IV females (raised on standard media) mated to IV-bwD males; mated D. simulans (bw/bw) females; and mated D. suzukii females. We chose these treatments as pheromones, CHCs and microbiotic profiles vary between species, and can also be vary within species depending on an individual’s diet (see Chandler et al. 2011; Fedina et al. 2012; Blum et al. 2013; Ferveur 2005; Han et al. 2017; Billeter and Wolfner 2018; Bing et al. 2018) and we wanted to see if these factors influenced egg-laying decisions (Schneider et al. 2012). We placed the dishes into the arenas ~2 h before the introduction of the focal flies (which occurred at 2:00 PM UTC/10:00 AM EST). The arenas (50 in total) were housed in a quiet, well-lit room. The number of focal females on each of the dishes was noted every half hour for a 5-h period and then summed to provide a measure of cumulative female dish counts. At the end of the observation period, petri dishes were collected, and the media from each dish was immediately transferred into standard culture vials containing 10 mL of standard media and placed into the incubator for 14 days. At that time, we counted the number and phenotype of all adult flies present in each vial. The offspring of focal IV-24 females were clearly distinguishable from other flies present (which either exhibited brown eyes, or SWD’s distinctive spotted wing/serrated ovipositor phenotypes). Since this first experiment revealed a strong bias for our focal (IV-24) females to oviposit on the IV-24 dish (see Results), we conducted a follow-up assay to determine whether this pattern was due to flies copying individuals of similar phenotype, or was instead due to the presence of some specific attractive cue produced by demonstrator females developing in a high-protein diet. In this follow-up assay following we collected flies and fly-cue dishes using the same protocols described above with the exception that this time we used focal females that were raised on a standard media rather than on the high-protein media. If flies were attracted to high-protein media associated cues, we would expect to see the same pattern displayed by the IV and IV-24 observer females (i.e., more oviposition on the IV-24 dishes). However, if flies were selectively copying those dished that contained cues from originated from individual of the greatest phenotypic similarity, we would expect the IV focal females to bias their attention toward the dish where the demonstrators were IV females mated to IV-bwD males. In this follow-up assay (which consisted of 45 replicate arenas), we counted the number of females on each dish every 30 min for 7.5 h and left the flies to oviposit overnight in the arenas for an additional 14 h (to increase egg yields), before collecting the dishes, and transferring the media to new vials so that the number of wild-type offspring could be counted 14 days later. Can females distinguish relevant oviposition-site cues? In our second experiment, we set out to measure habitat association (and oviposition behavior) in two groups of females (mated and virgin IV flies) that were presented with cues originating from groups of demonstrator conspecific D. melanogaster males or females that were either mated or unmated (virgin). Focal IV females were raised on standard media and collected as virgins within 8 h of eclosion from their pupae ~3–4 days before the start of the assay. Females in the mated treatment were housed in sets of 10 and combined with similarly aged IV males 22 h prior to the start of the assay. These males were removed (under light CO2 anesthesia) 2 h prior to the start of the assay, and mated females were returned to the vials. Virgin females were kept in sets of 10 until immediately before the start of the assay and lightly gassed 2 h prior to the start of the assay to ensure that anesthesia exposure did not confound our behavioral observations. Sets of 10 females were transferred into cafeteria-style arenas (described above) without anesthesia. In this experiment, we set up 40 replicate arenas using mated focal females and, and 38 arenas using virgin focal females. As above, each arena contained five petri dishes that potentially presented different cues (four fly-cue dishes and one control dish that had not been exposed to flies). The four fly-cue treatments were as follows: virgin females, mated females, virgin males, and mated males. Demonstrator virgin males and females were collected within 8 h of their eclosion from pupae, while demonstrator mated males were collected from mixed-sex vials 24 h prior to the start of the assay (thus had ~3 days to mate). For the dishes that were exposed to mated demonstrator females, we used IV females that mated with “spermless” males (described in Kuijper et al. 2006; Long et al. 2010). These males (lacking a Y-chromosome) can successfully court females and transfer normal amounts of seminal proteins but are incapable of transferring sperm, so their mates fail to produce any viable offspring (Ingman-Baker and Candido 1980; Chapman 1992). This allows us to unambiguously identify all offspring eclosing from these plates as being produced by the focal mated females, and removes any potential confounds associated with the presence of live larvae on the media. As above, the number of focal flies on each the different media dishes was recorded every 30 min for 6 h. Flies were left in the arenas overnight (15 h), and the media from all five dishes in mated female arenas were collected and then transferred to vials of fresh media. The number of flies eclosing from these vials was counted 14 days later. Statistical analyses All statistical analyses were performed using R.3.3.2 (R Development Core Team 2017). In our first experiment, we analyzed the effect of dish treatment on the cumulative number of female media dish visits by constructing generalized linear models (GLMs), with quasipoisson error distributions, where our response variable was the sum of all females observed on each dish within each arena tallied across all the 30-min intervals of the observation period. We used the Anova function in the car package (Fox and Weisberg 2011) to test whether the treatments means were different from each other using a log likelihood-ratio (LLR) chi-square test, followed by Tukey’s honestly significant difference (HSD) tests implemented by the glht function in the multcomp package (Hothorn et al. 2008) to determine the specific location of the differences between treatments. The number of offspring collected from each dish was also analyzed using the same the GLM procedure, except that the response variable was the total number of wild-type individuals that eclosed after 14 days from each dish. In our second experiment, we analyzed the variation in the cumulative number of females observed on each media dish within each arena using a GLM with quasipoisson error distribution, in which both focal female mating status (mated or virgin), media dish type and their interaction were independent variables. As there was a significant difference in the mean total number of dish visits made by mated and virgin focal females, we conducted additional comparisons of frequencies of specific media dish usage of the mated and virgin focal females by comparing the proportion of all flies observed on each media dish type between these two groups, standardized to the total number of counts for each individual arena. These comparisons were made using Mann–Whitey tests and were supplemented with Cliff’s delta statistics to determine effect sizes of the differences between groups. We also examined whether (for the arenas that had contained mated, ovipositing, females) there were any difference between dish types in the mean number of adult offspring that had eclosed using a GLM with quasipoisson error distribution. Results Can females distinguish between intra- and interspecific cues for suitable oviposition sites? In our first experimental assay, we compared the cumulative number of visits of IV-24 focal females (summed over 5 h) across treatment media dishes as well as the number of offspring eclosing as adults from each of the media dishes. Our analysis found that focal females exhibited heterogeneity in their mean cumulative dish counts (GLM; LLR χ 2 = 44.0, df = 4, P = 6.3 × 10−9), as they spent more time associating with the demonstrator media dishes compared to the control dishes (Figure 1i). The mean amount of oviposition on each of the types of media dish (measured as the number of eclosed focal phenotype offspring) was also heterogeneous (GLM; LLR χ 2 = 339.1, df = 4, P < 1.0 × 10−10), with IV-24 females laying virtually almost their eggs on the media dishes previously occupied by other IV-24 females (Figure 1ii). In our follow-up assay, where we used focal IV females raised on standard media, we also saw differences in mean cumulative dish counts (GLM; LLR χ 2 = 35.1, df = 4, P = 4.5 × 10−7) with females generally associating on the demonstrator media dishes more than the control media (Figure 1iii). The females also showed bias in their oviposition site choice (GLM; LLR χ 2 = 60.9, df = 4, P = 1.9 × 10−12) with significantly more oviposition activity occurring on IV-bwD dishes than any other of the demonstrator dishes, followed by the D. simulans dishes as the only other treatment that differed significantly from the control plates—including the IV-24 dish treatment (Figure 1iv). Figure 1 Open in new tabDownload slide Boxplots illustrating (i) the total number of IV-24 D. melanogaster females (reared on a high-protein media) seen associating with treatment patches in a arena, recorded every 30 min across a 5-h period, (ii) the total number of wild-type offspring that eclosed as adults from those media dishes. Media dishes had been previously exposed to either female D. simulans, D. suzukii, D. melanogaster from the IV population (raised on a high protein media “IV-24”) and mated to males from the IV-bwD, D. melanogaster from the IV population (raised on standard media) and mated to males from the IV-bwD population (“IV-bwD”), or had not been exposed to any flies (control). The bottom row figures (iii and iv) are as above with except that the focal IV females had been raised on standard media, and that observations were made over a 7.5-h period. The boxes enclose the middle 50% of data (interquartile range [IQR]), with the location of the median represented by a horizontal line. Values >±1.5 × the IQR outside the box are considered outliers and depicted as open circles. Whiskers extend to the largest and smallest values that are not outliers. Means sharing the same small letters in rows are nonsignificant at P < 0.05 according to Tukey’s HSD tests. Figure 1 Open in new tabDownload slide Boxplots illustrating (i) the total number of IV-24 D. melanogaster females (reared on a high-protein media) seen associating with treatment patches in a arena, recorded every 30 min across a 5-h period, (ii) the total number of wild-type offspring that eclosed as adults from those media dishes. Media dishes had been previously exposed to either female D. simulans, D. suzukii, D. melanogaster from the IV population (raised on a high protein media “IV-24”) and mated to males from the IV-bwD, D. melanogaster from the IV population (raised on standard media) and mated to males from the IV-bwD population (“IV-bwD”), or had not been exposed to any flies (control). The bottom row figures (iii and iv) are as above with except that the focal IV females had been raised on standard media, and that observations were made over a 7.5-h period. The boxes enclose the middle 50% of data (interquartile range [IQR]), with the location of the median represented by a horizontal line. Values >±1.5 × the IQR outside the box are considered outliers and depicted as open circles. Whiskers extend to the largest and smallest values that are not outliers. Means sharing the same small letters in rows are nonsignificant at P < 0.05 according to Tukey’s HSD tests. Can females distinguish relevant oviposition-site cues? In our second experiment, we compared the total number of counts (summed over 6 h) of mated and virgin focal females to different media dishes and counted the mean number of offspring of the mated focal females eclosing as adults from each type of media dish. Overall, we found that virgin females associated with media dishes more than did mated females (GLM mating treatment; LLR χ 2 = 13.6, df = 1, P = 2.2 × 10−4), there were differences in the mean total counts on the different media dishes (GLM patch treatment; LLR χ 2 = 1162.8, df = 4, P < 1.0 × 10−10), but there was no significant interaction between these two independent factors (GLM mating × patch treatment; LLR χ 2 = 3.5, df = 1, P = 0.47). A similar pattern was also seen in our comparisons of the proportion of cumulative female counts on each media dish type for the mated and virgin focal groups (Table 1). Both the virgin and mated females were more frequently observed on dishes previously exposed to virgin males (and more generally males) than they were on the control or the female dishes (Figure 2i,ii). We found significant differences in the number of offspring eclosing from the different dishes in the mated female treatment (GLM; LLR χ 2 = 54.2, df = 4, P = 4.9 × 10−11) where both the virgin and mated male media dishes had significantly more oviposition activity than either the control, the virgin female or the mated female dishes (Figure 2iii). Table 1 Comparisons of proportions of all observations made of virgin and mated D. melanogaster females on each of the different media dish types Media dish treatment . Mean proportion of all virgin females observed on dish . Mean proportion of all mated females observed on dish . Mann–Whitney . . Cliff’s Delta . 95% CI . . . . W . P . . . Control 0.05 0.07 959 0.05 0.26 (0.008, 0.484) Mated males 0.12 0.13 863 0.31 0.14 (−0.122, 0.376) Virgin males 0.72 0.65 605 0.12 −0.20 (−0.438, 0.055) Mated females 0.05 0.07 907 0.14 0.19 (−0.069, 0.430) Virgin females 0.06 0.07 900 0.16 −0.18 (−0.079, 0.423) Media dish treatment . Mean proportion of all virgin females observed on dish . Mean proportion of all mated females observed on dish . Mann–Whitney . . Cliff’s Delta . 95% CI . . . . W . P . . . Control 0.05 0.07 959 0.05 0.26 (0.008, 0.484) Mated males 0.12 0.13 863 0.31 0.14 (−0.122, 0.376) Virgin males 0.72 0.65 605 0.12 −0.20 (−0.438, 0.055) Mated females 0.05 0.07 907 0.14 0.19 (−0.069, 0.430) Virgin females 0.06 0.07 900 0.16 −0.18 (−0.079, 0.423) Medians of proportions were compared using the nonparametric Mann–Whitney test, as well as the Cliff’s delta effect size statistic. CI, Confidence interval. Open in new tab Table 1 Comparisons of proportions of all observations made of virgin and mated D. melanogaster females on each of the different media dish types Media dish treatment . Mean proportion of all virgin females observed on dish . Mean proportion of all mated females observed on dish . Mann–Whitney . . Cliff’s Delta . 95% CI . . . . W . P . . . Control 0.05 0.07 959 0.05 0.26 (0.008, 0.484) Mated males 0.12 0.13 863 0.31 0.14 (−0.122, 0.376) Virgin males 0.72 0.65 605 0.12 −0.20 (−0.438, 0.055) Mated females 0.05 0.07 907 0.14 0.19 (−0.069, 0.430) Virgin females 0.06 0.07 900 0.16 −0.18 (−0.079, 0.423) Media dish treatment . Mean proportion of all virgin females observed on dish . Mean proportion of all mated females observed on dish . Mann–Whitney . . Cliff’s Delta . 95% CI . . . . W . P . . . Control 0.05 0.07 959 0.05 0.26 (0.008, 0.484) Mated males 0.12 0.13 863 0.31 0.14 (−0.122, 0.376) Virgin males 0.72 0.65 605 0.12 −0.20 (−0.438, 0.055) Mated females 0.05 0.07 907 0.14 0.19 (−0.069, 0.430) Virgin females 0.06 0.07 900 0.16 −0.18 (−0.079, 0.423) Medians of proportions were compared using the nonparametric Mann–Whitney test, as well as the Cliff’s delta effect size statistic. CI, Confidence interval. Open in new tab Figure 2 Open in new tabDownload slide Boxplots illustrating the total number of counts of D. melanogaster females on different media dishes, recorded every 30 min over a 6-h period for (i) virgin and (ii) mated females, and (iii) the total number of IV offspring that eclosed as adults from media dishes that were produced by the mated focal females. Media dishes had been previously exposed to female or male D. melanogaster of different mating statuses (mated or virgin) or had not been exposed to any flies (control). Boxplot components are as in Figure 1. Means sharing the same small letters in rows are nonsignificant at P < 0.05 according to Tukey’s HSD tests. Figure 2 Open in new tabDownload slide Boxplots illustrating the total number of counts of D. melanogaster females on different media dishes, recorded every 30 min over a 6-h period for (i) virgin and (ii) mated females, and (iii) the total number of IV offspring that eclosed as adults from media dishes that were produced by the mated focal females. Media dishes had been previously exposed to female or male D. melanogaster of different mating statuses (mated or virgin) or had not been exposed to any flies (control). Boxplot components are as in Figure 1. Means sharing the same small letters in rows are nonsignificant at P < 0.05 according to Tukey’s HSD tests. Discussion Copying is a strategy used in many species faced with making choices including decisions about habitat, food, and/or mates (Valone and Templeton 2002; Galef and Laland 2005; Godin et al. 2005; Wertheim et al. 2005; Parejo et al. 2006; Valone 2007; Grüter and Leadbeater 2014). In doing so, individuals avoid the costs incurred with personally sampling their environment by instead relying on the observed outcomes of decisions made by others (Valone 2007). For copying to be an adaptive strategy, it is essential that those who copy others are able to recognize the relevant/meaningful public information signals in their environment (Depetris-Chauvin et al. 2015), as random copying can result in decreased fitness (Boyd and Richerson 1985; Laland 2004; Kendal et al. 2009). In our study, we set out to examine the nature of oviposition site-copying in the fruit fly D. melanogaster, which is increasingly being used as a model for studying social information use, by examining the specificity of its social information usage. This was done through a series of experiments designed to determine whether ovipositing females would copy the behavior of different groups of demonstrators whose public information cues potentially provide varying degrees of relevant information about oviposition-site suitability. Our assays revealed that D. melanogaster egg-laying behavior is strongly influenced by the presence and type of signals left behind by demonstrators, but that this phenomenon may not be a straight-forward case of copying behavior. While females in our first set of assays showed affinity for cues from conspecific demonstrators that had been raised in a similar environment, in our second assay, where females encountered cues from males and female demonstrators of different mating statuses, they did not behave in a manner that was strictly consistent with behavioral copying. Here, we discuss how our results fit within the scope of social and public information theory and what they tell us about the potential for future studies of copying behavior in D. melanogaster. In our first set of assays, we set out to quantify the precision of the oviposition-site copying behavior of D. melanogaster by observing how females responded to a variety of social cues originating from heterospecific Drosophila as well from conspecific D. menanogaster that had been raised in different environments. We had predicted that if oviposition-site copying behavior was indeed an adaptive phenomenon (Galef and Giraldeau 2001), then focal female flies would selectively use socially acquired information produced by those demonstrators who were the most similar to themselves, as this public information may be the most relevant and beneficial to their fitness. Both assays in our first experiment provide support for this prediction. Although focal females largely showed similar levels of interest in all scented patches (Figure 1i,iii), they oviposited significantly more eggs on those patches that had been exposed to demonstrator conspecifics that had also developed on the nutritional environment that matched that of the focal females (Figure 1ii,iv). This pattern was observed in both our first assay where focal females had been raised on high protein media, as well as in the follow-up assay where the females had developed on standard media, ruling out the possibility that the pattern observed in our first assay could be attributed to the presence of a unique attractant associated with demonstrators developing on the high protein media. While this biased pattern was more pronounced in our first assay compared to our second assay, this is probably the result of a more distinctive set of cues produced by flies developing on the unusual (for our lab) high-protein media, compared to those produced by the other demonstrator flies that all developed on media of the same type. These results suggest that D. melanogaster females are discerning in their use of public information, and are also plastic in which cues are used. Drosophila are sensitive to the olfactory cues presented by others (Duménil et al. 2016), and use cues associated with diet when making mate choice decisions (Najarro et al. 2015), as well as when distinguishing between kin and non-kin (e.g., Lizé et al. 2014; Martin and Long 2015). As D. melanogaster can develop under a wide range of conditions (Cavicchi et al. 1995; Chippindale et al. 1996), which may favor different phenotypes (McCabe and Partridge 1997), copying the behavioral decisions of individuals who are most similar to themselves may be the best means of making a decision that will yield the greatest fitness benefits (Wagner and Danchin 2003). In our second experiment, we focused our attention on how females responded to patches that had been exposed to either males or females of differing mating status—the surprising result of which has led us to question the fundamentals of copying behavior in D. melanogaster. As with our previous experiment, we predicted that if oviposition-site copying behavior was adaptive, then focal female flies would show bias toward socially acquired information produced by those demonstrator individuals who were the most similar to themselves, as a way to obtain information that is most potentially relevant to their success. Specifically, we predicted the source of the most relevant information on mated females seeking suitable oviposition sites would presumably have originated from mated female demonstrators (who likely produce a distinctive mixture of CHCs, male pheromones and female microbial cues that are ejected during oviposition; Duménil et al. 2016). Instead, we observed that our mated focal females primarily associated with media that had previously kept virgin males (Figure 2ii), and had laid more eggs on those media dishes exposed to males than they did on other media patches (Figure 2iii). The patches that had been exposed to mated females were among the least associated and oviposited, and were not significantly different from our unscented control patches. This result would seemingly challenge a key assumption of copying oviposition site behavior in D. melanogaster, that individuals will copy those that are most similar to themselves (Laland 2004). Our results contrast with some of the findings of Duménil et al. (2016) wherein a two-choice assay, females laid more eggs on media that had been exposed to a mated female demonstrator than on an alternative media which had been exposed to either virgin males, mated males, or virgin female demonstrators. The reason for this discrepancy is not known, but might be due to differences in our fly populations (i.e., the signals they present, or in in their use of public information) or in our experimental methods. When comparing methods, we see two possibilities. First, the demonstrator (and observer) flies used by Duménil et al. (2016) were several days older than those used in our assays. The types and amount of CHCs expressed by D. melanogaster individuals can change over a matter of days (Everaerts et al. 2010; Kuo et al. 2012), which raises the possibility that the observer females in our two assays experienced may not have experiences the same choice of cues. A second possibility is that our use of mating females to spermless males may have affected the cues left behind by these demonstrators, as they would not have been able to eject sperm onto the surface of the media (as described in Duménil et al. 2016), which might act as a cue to prospective ovipositors. This difference, however, does not explain why sites previously exposed to virgin males had such a great appeal to mated (and virgin) compared to all others. A further unexpected result came from our comparison of the behavior of virgin and mated females in our assays, as we observed no significant differences in the frequencies of patch use between these two groups (Figure 2i,ii, Table 1). We had predicted that if mated females were engaging in copying behavior to locate suitable oviposition sites, then their social information use would differ from that of virgin females as their nutritional preferences differ (Ribeiro and Dickson 2010; Camus et al. 2018). However, our results suggest the presence of social cues may have an over-riding influence on what might otherwise be adaptive feeding behaviors, similar to what was seen in both Golden and Dukas (2014) and Duménil et al. (2016) where female preference for certain conspecific cues led them away from more nutritious options. A distinct possibility raised by our second experiment is that if females of different mating statuses do not behave differently while looking for oviposition sites, or seek out signals originating from other similar conspecific demonstrators, it may not be appropriate to characterize this as “copying” behavior, an idea we address below. Overall, our results are generally consistent with previous studies that female fruit flies use social information when choosing an oviposition site (Sarin and Dukas 2009; Battesti et al. 2012; Golden and Dukas 2014), and that they exhibit specificity in their perception of cues. However, contrary to our a priori prediction that females would use cues from other females when choosing oviposition sites, they instead appeared to value cues from males, and did not change their behaviour depending on their own mating status. If females are using social information when making decisions, is that enough to classify this is as copying behavior? In Valone and Templeton’s review of social learning (2002) they stress the differences between public and social information. Social information is obtained before an individual visits and evaluates a resource and is often used to share the location of resources but does little to describe the quality of the resource. In contrast, public information is collected at a site by evaluating the attempts and successes of others to better assess the quality of the resource. Female D. melanogaster may gain public information through direct observation of other females ovipositing (as in Sarin and Dukas 2009 and Battesti et al. 2012), or the presence of larvae (as in our first experiment, and in Golden and Dukas 2014) that would alter their own behavioral decisions. In contrast, in our experiments, the cues present on the patches (eggs, male-derived cVA, CHCs, and/or microbial cues left behind by males and female demonstrators) may be social, and not public information. Thus, we raise the possibility that true copying behavior may depend on the use of public rather than social information, and that in future studies great care should be taken to ensure that experimental designs incorporate the former and not the latter. In the wild, there may be considerable heterogeneity in the availability and quality of oviposition sites that are available to female D. melanogaster (Reaume and Sokolowki 2006; Markow 2015), and in the types of cues present at the sites they encounter. The ability to recognize habitat usage by conspecifics, especially those who developed in a similar nutritional environment, may be of adaptive value to ovipositing females, as this may decrease the probability that their offspring will compete with larvae from another species (Barker 1971; Atkinson 1979). What value might a female gain by choosing to oviposit at a site that had previously been used by males instead of females? On one hand, she may be missing out on suitable developmental environments for her offspring, but in the context of mate choice copying, Nordell and Valone (1998) have argued that for individuals who are unable to make their own assessments, copying others yields the same chance of success as choosing randomly. If males are capable of locating suitable habitats for offspring development, then females that use male cues will end up choosing better sites for oviposition, and can improve their reproductive success above chance levels. The ability to locate females that are receptive to mating is an important source of variation in individual reproductive success in male fruit flies (Pischedda and Rice 2012) and male seek out food sites (Lebreton et al. 2012), not for feeding, but for the opportunity to court with arriving females, who spend much less time on these sites than males (Spieth 1974). There is likely strong selection on males to be able to locate suitable feeding (breeding) sites and thus male signals might ultimately prove to be a source of reliable information about the quality of a potential oviposition site, and females’ attraction to these sites may reflect an adaptive use of public information. Alternatively, the focal females may be gravitating toward the male-associated cues, as they are seeking prospective mates with the intention of mating for the first time (for virgin females) or replenishing sperm supplies and/or “boosting” their fecundity through an extra dosage of Accessory Gland Proteins (ACPs) for the mated females (Long et al. 2010). The bias toward virgin male cues may be to avoid mating with males who have depleted sperm and/or ACP reserves (Demerec and Kaufmann 1941, Sirot et al. 2009). Another possibility is that the focal females did not use the cues left behind by the demonstrators and instead based their decisions on the behaviors of the other focal females present within the observation arena, the prospect of which has been raised in previous studies (Sarin and Dukas 2009, Battesti et al. 2012). While interactions between individuals might influence some of the observed patterns of biased patch usage though the process of collective selection (Lihoreau, Clarke, et al. 2016) if these biases did arise via positive feedback loops (sensu Wagner and Danchin 2003), then the identity of the preferred patch within an arena would be arbitrary and randomly vary from arena to arena. The consistency of the patch usage patterns across our independent, replicate arenas likely indicates that cues present on the media surface are of primary importance to the behavioral decision mated by each of the focal females. Future studies might test for the potential effect of social interactions of other ovipositing females by separating females into smaller individual test chambers with the same media options. It may also be worth revisiting earlier experiments by Battesti et al. (2012) and Sarin and Dukas (2009) that used isolated aggregate pheromone as male signals and replaced it with a more complete male signal as this may have a stronger effect than they found from cVAs alone. These future studies may deepen our understanding of the causes and consequences of why female behaviors differ in response to social cues and through interactions between conspecifics. The authors wish to acknowledge the help provided by all the “fly-pushers” in the Long lab; T.A.F.L. was funded with a Natural Sciences and Engineering Research Council of Canada (NSERC) Discovery grant, and H.M. received additional funding from the Faculty of Graduate and Postdoctoral Studies at Wilfrid Laurier Univerity (WLU). The authors would like to extend thanks to Dr. Scott Ramsay and Dr. Derek Grey and Natasha Gallo for their advice and insight. This work was conducted at WLU, which exists on the traditional territory of the Neutral, Anishnawbe, and Haudenosaunee peoples. Authors’ contributions: The experiment was conceived and executed by TAFL and HLM who also collaborated on the data analysis and the writing of the manuscript. Conflict of interest: The authors declare no conflict of interests. Ethics: This study did not require approval from an ethics committee. Data accessibility: Analyses reported in this article can be reproduced using the data provided by Malek and Long (2020) References Atkinson WD . 1979 . A field investigation of larval competition in domestic Drosophila . J. Anim. Ecol . 48 : 91 – 102 . Google Scholar Crossref Search ADS WorldCat Avarguès‐Weber A , Dawson EH, Chittka L. 2013 . Mechanisms of social learning across species boundaries . J. Zool . 290 : 1 – 11 . Google Scholar Crossref Search ADS WorldCat Ayala FJ , Ayala M. 1969 . Oviposition preferences in D. melanogaster . Dros. Inf. Serv . 44 : 120 . OpenURL Placeholder Text WorldCat Barker JS . 1971 . 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TI - On the use of private versus social information in oviposition site choice decisions by Drosophila melanogaster females
JO - Behavioral Ecology
DO - 10.1093/beheco/araa021
DA - 2020-06-19
UR - https://www.deepdyve.com/lp/oxford-university-press/on-the-use-of-private-versus-social-information-in-oviposition-site-XK0uH6LG6c
SP - 739
VL - 31
IS - 3
DP - DeepDyve
ER -