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. 2018 Aug 11;29(6):1409–1414. doi: 10.1093/beheco/ary114

Past and present resource availability affect mating rate but not mate choice in Drosophila melanogaster

Erin Tudor 1, Daniel E L Promislow 1,2, Devin Arbuthnott 3,✉
PMCID: PMC6293226  PMID: 30568395

The choice of when to mate can change rapidly based on changes in the environment. We show that the mating rate of male fruit flies (Drosophila melanogaster) decreases when starved, but can rapidly increase when males find females in high-quality environments. Therefore, mating decisions can change quickly and are strongly influenced by changes in environment.

Keywords: condition-dependence, mate choice, phenotypic plasticity, starvation

Abstract

The choices of when, where, and with whom to mate represent some of the most important decisions an individual can make to increase their fitness. Several studies have shown that the resources available to an individual during development can dramatically alter their mating rate later in life, and even the choice of mate. However, an individual’s surroundings and available resources can change rapidly, and it is not clear how quickly the redistribution of resources towards reproduction can change. To address this important question, we measured mating rate and mate choice among Drosophila melanogaster males that were manipulated in terms of both past resources (control vs. starvation) and the resources available during mate choice (food vs. no food). We found that males given access to ample resources prior to mate choice showed higher mating rates than those that were starved, in agreement with previous studies. However, we also found that this effect can be reversed quickly, as starved males given the opportunity to mate in a high-quality environment mated at frequencies equivalent to their fed counterparts. Although past and present resources affected mating rate, they did not affect mate choice, as males mated with high-quality females at high frequencies regardless of their condition and environment. Our results show that both current condition as well as the promise of future resources can dramatically influence individuals’ investment into reproduction and that such mating decisions are extremely plastic and reliant on environmental cues.

INTRODUCTION

The choice of when and with whom to mate can have profound impacts on an individual’s fitness and, therefore, represents a crucial set of decisions for both males and females (Andersson 1994). First, because resource availability fluctuates within and between environments, the choice of when and where to mate can influence both the number and fitness of potential offspring that can be produced, as well as the resources available for future reproductive opportunities. As a consequence, individuals should only mate if their past and present environments align to support advantageous reproductive conditions. Second, the choice of whom to mate can greatly affect the number and fitness of offspring produced, depending on both the genetic quality and the condition of potential mates (Zahavi 1975; Rowe and Houle 1996; Iwasa and Pomiankowsky 1999; Arbuthnott et al. 2017). However, mate searching, mate choice, and courtship can be energetically costly endeavors (Andersson 1994; Kotiaho et al. 2001; Whitlock and Agrawal 2009; Gibson and Uetz 2012). Therefore, as with the choice of when and where to mate, the choice of whom to mate and overall choosiness can be strongly influenced by an individual’s condition and available resources. Despite the potential importance of past and present resource availability to these critical mating decisions, relatively little is known about how available resources influence specific mating decisions (when and with whom to mate), or how plastic condition-dependent decisions are.

With respect to the decision of whether to mate at all, current theory and evidence suggests that individuals mate and/or court less when they have been raised in a nutrient-poor environment (Blay and Yuval 1997; Engqvist and Sauer 2001). For example, male wolf spiders raised in nutrient-poor environments courted less than males raised in nutrient-rich environments (Gibson and Uetz 2012). Related to this trade-off, when male guppies were simultaneously given the opportunity to court or feed, they prioritized feeding (Abrahams 1993). These results are in agreement with the widespread observation that reproduction appears to trade-off with functions of somatic maintenance, and that low-condition individuals preferentially direct their limited resources towards nonreproductive processes (Hunt et al. 2004; Ja et al. 2009; Arbuthnott et al. 2016). Additionally, offspring produced in a low-quality environment (those with fewer available resources and/or more stressors to overcome) may have lower fitness as a result (Kotiaho et al. 2001). Therefore, present and future resource availability, in addition to past resource acquisition, can have large impacts on the survival and reproductive potential of produced offspring, meaning individuals may use potential resource availability in addition to information about their own condition when making decisions about where and when to mate. However, though it has been shown that, on average, individuals mate less when in poor condition, it is currently unknown whether individuals can use information from a changing environment to alter their mating decisions, and if so, how quickly they can alter behavior in response to this new information. Previous studies have shown that survival rates respond almost immediately to changes in nutrient availability, increasing when fruit flies are transferred from high-nutrient to low-nutrient food (Good and Tatar 2001; Mair et al. 2003). Can such rapid physiological changes extend to behavioral alterations? Rapid environmental changes can have large impacts on sexual selection, though these have not been adequately considered in sexual selection research (Cornwallis and Uller 2010; Bonduriansky 2014).

In addition to the choice of when and where to mate, the choice of whom to mate can also provide direct or indirect benefits to both sexes. Direct benefits include males choosing high fecundity females (Long et al. 2009; Arbuthnott et al. 2017) or females choosing males offering large nuptial gifts (Vahed 1998), increasing the reproductive resources available. Indirect benefits include mechanisms that may increase the fitness of offspring by choosing mates of high genetic quality (good genes), genetic compatibility, or increased attractiveness that will be inherited by offspring (sexy sons; Andersson 1994). Given the choice of potential mates, it is often predicted that individuals should choose the most fit individual, assessed via honest indicators of genetic and environmental quality (Zahavi 1975; Rowe and Houle 1996; Iwasa and Pomiankowsky 1999), which in turn will ensure that offspring production will be maximized and/or high fitness offspring will be produced. For example, female fecundity is often correlated with honest indicators in many species such as larger size in fruit flies (Byrne and Rice 2006), or more colorful wings in the cabbage butterfly (Tigreros et al. 2014).

Though it is common for poor condition individuals to mate less, it is currently unclear how condition affects the choice of whom to mate for both males and females. On one hand, individuals in low condition might display greater mating preferences for high-quality mates because they must invest their limited resources more wisely when mating, given their limited mating opportunities. On the other hand, low-condition individuals may show less choosiness during mate choice to avoid the costs of mate searching and assessment. In agreement with the first hypothesis, resource-depleted males have a stronger preference for larger females than nondepleted males in fruit flies (Byrne and Rice 2006). Furthermore, poor condition male scorpionflies invest more in matings with high-quality females than their high-condition counterparts (Engqvist and Sauer 2001).

Mating rate and mate choice may also change based on environmental quality as a byproduct of physiological changes under starvation. For example, when starved, Drosophila melanogaster show an increased sensitivity to attractive odors, in this case food (Farhadian et al. 2012). This result raises the question of whether this increased sensitivity to attractive odors may be applied in the context of choosing mates, since individuals of both sexes in fruit flies rely on chemical signals to detect and choose mates (Jallon 1984). Therefore, starvation-induced changes in chemosensory sensitivity could enhance the abilities of individuals to detect and choose mates. However, the associated decrease in available resources following starvation may encourage individuals to delay mating or decrease investment in mate choice. It is therefore unclear how starvation might influence mating rate and mate discrimination.

Females are traditionally thought to be the choosier sex, with males simply maximizing number of matings rather than quality of mates. This follows from the fact that individual eggs require more investment and provisioning than individual sperm (Bateman 1948). Given their smaller investment in offspring, males are often expected to be indiscriminate in mate choice, and as a result, male choice often goes unmeasured in sexual selection research. Despite this common view, males have been shown to display mating preferences in many species (Bonduriansky 2001; Edward and Chapman 2011), and advantageous mate choices can increase males’ offspring production by selecting more fecund females (Arbuthnott et al. 2017). Also, despite the smaller investment in gametes, males do invest in mating through courtship, sperm and accessory protein production, and in some cases even provide nuptial gifts. Arbuthnott et al. (2017) recently found that male D. melanogaster show consistent and advantageous mate choice when choosing among repeatable female genotypes, even when females are rendered inactive. Based on these results, and the easily measurable direct benefits of adaptive male mate choice, we focused on male mate choice in this species to address the following questions: 1) Is mating rate altered in response to low condition/starvation of males? 2) Do past vs. present available resources alter mating decisions and outcomes in a plastic way? and 3) Do starved males mate with more fecund females at a different rate than control males?

To address these questions, we carried out a series of mate choice assays in the fruit fly D. melanogaster. We manipulated males’ access to food at 2 time points, prior to mate choice, and during mate choice. We therefore gave high- and low-condition males the opportunity to mate and exert mate choice both in the presence and the absence of additional resources. Although we manipulated male starvation status, and set out to measure male mate choice by giving individual males the choice between 2 females, we must acknowledge that changes in female behavior could also potentially alter the outcomes of mating trials. Nonetheless, our manipulations and measures allow us to measure the importance of rapid environmental changes on mating rate and mating behavior. Overall, we found that low-condition males had reduced mating rates, but only when the opportunity to mate occurred in the absence of food. Low-condition males given the opportunity to mate in the presence of food, as well as high-condition males in both environments, displayed high mating rates. Therefore, both past and present resource availability is influential in the decision of when and whether to mate. However, neither past condition nor mating environment influenced mate choice, as mated males always showed high preference for more fecund female genotypes.

MATERIALS AND METHODS

Fly stocks

All D. melanogaster used were from the stock population Canton-S and from 2 inbred lines from the Drosophila Genetic Reference Panel (DGRP; MacKay et al. 2012), Ral-362 and Ral-774. Ral-362 and Ral-774 were used because females from these lines showed consistent differences in attractiveness and offspring production (Arbuthnott et al. 2017). The Canton-S population was provided by the Pletcher lab at the University of Michigan, and DGRP lines were ordered from the Bloomington Stock Center. These stocks were maintained on Caltech (CT) food, in incubators kept at 24o C, 50% humidity, and a 12:12 h light:dark cycle.

Collection

Virgins of each line were collected within 8 h of emergence under light CO2 anesthesia. Females of lines Ral-362 and Ral-774 were collected at 10 females per vial, whereas males of Canton-S were collected at 7 males per vial. All males were collected within 1 day of each other, and females were collected over 2 days.

Food availability treatments

To assess the impact of food on mating rates and outcomes, we manipulated males’ access to food prior to and during mate choice assays in a 2 × 2 factorial design (food present/absent before mate choice × food present/absent during mate choice). After collection as virgins, we kept males on food for 24 h to allow them to improve their body condition after emergence as adults. After this, we moved half of the males to starvation treatment vials, which were filled with 2% agar media that offers no nutritional benefit, whereas the other half of males were kept in control vials filled with CT food. To control for the movement of starvation treatment males, we tapped the vials containing control males on the counter to simulate movement to new vials. Males were held in their starvation or control vials for 48 h prior to mate choice assays. Farhadian et al. (2012) found that this amount of time was sufficient to elicit a starvation correlated response in chemosensory ability in D. melanogaster. After 48 h of starvation or control conditions, males were moved to mate-choice assays, in vials either with food or with 2% agar (vial treatment). All females were kept under standard (nonstarvation) conditions prior to mate choice assays. Therefore, while males were manipulated via food availability at 2 time points (before/during mate choice), females were manipulated at only 1 time point (during mate choice).

Mate-choice assay

We measured mating rates and mate choice by giving Canton-S males from each treatment (food present/absent before mate choice × food present/absent during mate choice) the choice between 2 DGRP females from different lines. We used the lines Ral-362 and Ral-774 because in previous mate choice experiments Ral-362 was chosen consistently over Ral-774 by males of several genetic backgrounds, including Canton-S under normal feeding conditions (Arbuthnott et al. 2017). Additional assays showed that male mate choice among inbred lines was maintained even when females were inactive, and therefore these mate choices are male-driven and not solely due to differences in female receptivity (Arbuthnott et al. 2017). We further showed that such mate choice is not influenced by infection by Wolbachia (Arbuthnott et al. 2016). By using these 2 lines, we can determine whether mate choice deviates from the established pattern under starvation conditions. We labeled females using red and yellow fluorescent powder 24 h prior to the mate choice assay. Mate choice assays were color-balanced, such that each line was red in half of the trials, and yellow in the other half. One Ral-362 and one Ral-774 female were placed in each vial at 07:00 the morning of the mate choice assay and allowed to acclimate for 1 h. At this point, we initiated mating assays by adding 1 male to each vial and observing each trial for mating for up to 2 h. When a mating occurred, we recorded the vial number and color of the female mated, which allowed us to determine the mated female’s identity. As such, we measured the mating rate for each treatment, and the mate choice of each mated male. Each male was only used in a single mate choice trial.

We ran 3 replicate mate choice assays to determine repeatability. During the first replicate, based on an assumption that starved males would mate less, we set up more trials for this treatment to accurately assess mate choice (starved and tested on agar n = 194, starved and tested on food n = 193), while fed males were set up in smaller numbers (fed and tested on food n = 49, fed and tested on agar n = 48). After the first replicate, it was determined that despite being starved the flies had relatively high mating rates, so we balanced sample sizes across starvation treatment for subsequent replicates. In replicate 2, we set up 75 trials of each treatment; whereas in replicate 3, we set up 100 trials of each treatment.

Statistical analysis

We ran a generalized linear mixed model with a binomial distribution to analyze the results of the mate choice assays. We first analyzed the occurrence of mating in all the trials (mated or unmated). We then analyzed male mate choice using only the trials where mating had occurred and determined whether the male had mated with the more attractive female or not. In both analyses, the result was a binomial response (mated vs. not mated, attractive female mated vs. unattractive female mated), with the starvation treatment, mating vial treatment, and their interaction modeled as fixed effects, and replicate number modeled as a random effect.

RESULTS

Resource availability and mating rate

Mating rates were lower for males who were starved for 48 h in the absence of food (agar vial treatment), compared to starved males in the presence of food, a pattern repeated in all replicates (Figure 1). In contrast to starved males, fed males had high mating rates in both the presence and absence of food (Figure 1; starvation × vial treatment interaction z1 = −4.5, P = 6.8 × 10–6).

Figure 1.

Figure 1

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The proportion of males that mated with any female (± SE) for all replicates (1–3). Mating rates were measured either in the presence of agar (dark bars) or food (white bars).

There were also significant effects of vial treatment (z1 = 7.6, P = 2.0 × 10–14), with mating rates lower in the presence of agar, and starvation treatment (z1 = 5.6, P = 2.8 × 10–8), with fed males mating more. Our results show that recent resource availability has significant effects on mating rate. However, it is not only past access to food which can drive increases in mating rates, but also sudden changes in resource availability, as starved males showed increased mating when exposed to food during mating opportunities.

Resource availability and female attractiveness

Replicate one showed a trend for the vial × starvation treatment interaction affecting mate choice (z405 = −1.7, P = 0.093), where fed males in the presence of food mated with unattractive/lower fecundity females more often than any other treatment. However, this result was not repeated in subsequent replicates (Figure 2), and there were no overall significant effects of starvation treatment (z1 = −0.8, P = 0.42), vial treatment (z1 = −1.1, P = 0.28), or interaction between the 2 (z1 = −0.79, P = 0.43) on the frequency that males mated with more attractive females. It is likely that the second and third replicate better represent effects of starvation on choosiness and that neither starvation state nor vial media have a significant effect on mating biases when males are given the choice between females.

Figure 2.

Figure 2

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The proportion of mated males that mated Ral-362 females (± SE) for all replicates (1–3). Mating rates were measured either in the presence of agar (dark bars) or food (white bars).

DISCUSSION

We found that the mating rate of starved males is affected by the combination of their starvation state and the presence of food (Figure 1). Although fed males mated consistently, regardless of their vial media, starved males were more likely to mate in the presence of food. The change in mating rate of starved males in the presence of food indicates that males could be displaying rapid plasticity in mating decisions based on resource availability. Males have previously been shown to alter mating probabilities when in a resource limited environment (Blay and Yuval 1997; Miller and Brooks 2005). However, in opposition to our findings, there are also cases where low-nutrition males are more eager to mate than high-nutrition males (Tigreros et al. 2014). Our data show that decisions regarding investment in mating are more complicated than simply relying solely on the past resource availability and present physiological condition. Although the starved males mated significantly less when on agar than on food, the fed males did not differ in their mating rates between these environments. Since we only observed changes in mating rate among starved males, one possibility is that the starved males are trading off mating opportunities for somatic maintenance and longevity when food remains absent during mating opportunities, waiting on the possibility that there will be a better opportunity when food does become available. However, the starved males who are introduced to such increases in food availability rapidly increase their mating rate, possibly capitalizing on the future resource gains their new environment will afford without sacrificing somatic maintenance in this improved situation.

Another possible, but related, explanation for our observation is that females altered their mating receptivity based on the mating environment, and starved males were less able to overcome decreases in receptivity. It may be that, when the mating assay occurred on food, females were more receptive to mate and the males did not need to court or harass the female as vigorously to induce mating. However, when mating assays were performed in the absence of food, females may have lowered their receptivity, and starved males did not have adequate resources to increase their courtship or harassment activity to accommodate these changes. The ability of a male to successfully court and mate, when nutrient deprived, has previously been shown to affect his mating success (e.g. Gibson and Uetz 2012), and females have been shown to decrease receptivity when nutrient deprived (Eraly et al. 2009; Rosenthal and Hebets 2015), and exert greater mate choice in these conditions (Ortigosa and Rowe 2002). It is possible that the past and present environments of males and females combine to make it more difficult for low condition males to achieve matings with reluctant females. While we cannot disentangle these possibilities with our data, it would be possible to test for the role of female reluctance in environment-induced decreases in mating rate by measuring male courtship toward inactive females in these different environments, as in Kuo et al. (2012) and Arbuthnott et al. (2017). Regardless of the mechanism underlying this change, our data show that mating probabilities can change rapidly in response to changing environments.

Although the proportion of matings that occurred was significantly tied to the starvation treatment and mating environment, the type of female (Ral-362 or Ral-774) mated was not affected by either starvation state or the media on which the mate choice trial took place. We had predicted that, because the sensitivity to attractive odors like food can be affected by starvation, male olfactory sensitivity might be extended to evaluating sexual signals. In addition to this physiological mechanism, it is also possible that low resource availability increases male motivation to display choosiness, as the importance of mating with a high-quality mate may be altered if male resources are limited, leading to lower overall mating opportunities. One possible explanation for our null result is that if males do invest in mating at all they invest in the more profitable female, regardless of their condition. Male D. melanogaster have been shown to be limited in their ability to mate successively and to maintain a high level of choosiness throughout their lives (Baxter et al. 2014). Additionally, males in any environment possess limited resources to put towards mating (Engqvist and Sauer 2001; Byrne and Rice 2006; Miller and Brooks 2016). In this light, it is often in the best interest of the male to consistently choose the highest quality female that is available. The consistently high level of mating with the more attractive female genotype (Ral-362) in males across treatments is in line with this theory, as the preferred female genotype is in fact more fecund than the alternative (Arbuthnott et al. 2017). One possible reason for consistent mate choice is that males of this species use multiple traits, including chemical and visual cues, to determine attractiveness (Arbuthnott et al. 2017), and changes in chemosensory sensitivity alone do not significantly change the ability to choose the more attractive female. Another potential mechanism underlying such stable mate choice is invariant differences in female receptivity among the inbred lines used. Our previous assays showed that male choice between inbred female lines persists even when females are inactive, and therefore mate choice is not solely dependent on female receptivity (Arbuthnott et al. 2017). However, we did not assess this aspect of female attractiveness in this assay, and it remains possible that female receptivity partially drives the constant male mating biases between these female lines.

Overall, we found that the resource dependence of mating decisions appears to be quite plastic. Resources both past and present have shown themselves to influence mating behavior. Males have lower mating rates when they are in low condition. However, starved males reverse this trend and had increased mating rates when resources quickly become available. Males were not given enough time to eat new food and increase their condition, but instead increased mating rates on the expectation of increased condition in the future. This suggests that males are either more likely to reserve resources for nonreproductive activities and future reproductive opportunities under low condition or are unable to mate females while they are in low condition, but will rapidly redirect available resources to reproduction when the environment changes or when females become more receptive. However, this increased investment in reproduction did not influence the choice of whom to mate. All mating males, regardless of starvation status or mating environment, overwhelmingly mated with the more attractive and more fecund female when given a choice. Female assessment and choice may not be costly in the mate choice environment we provided, which would allow advantageous mate choices regardless of male condition. Alternatively, if males have decided to invest in mating, they might commit to maximize their investment by mating with the most fecund female, regardless of the resources required. Future work is necessary to separate these alternative hypotheses, as well as to assess the fitness and life history consequences of altering mating rates based on environmental changes.

FUNDING

This work was funded by NIH grant GM102279 to D.P. and through a NSERC postdoctoral fellowship to D.A.

Acknowledgments

We are grateful to Quynh Tran, Alexandria McCarthy, Laurie Huang, and Sharon Ornels for help carrying out this experiment. The Promislow lab at the University of Washington provided valuable feedback and advice throughout the planning and implementation of this project.

Data accessibility: Analyses reported in this article can be reproduced using the data provided by Tudor et al. (2018).

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