Author response: A fitness trade-off between seasons causes multigenerational cycles in phenotype and population size

Full text Figures and data Side by side Abstract eLife digest Introduction Results Discussion Materials and methods Appendix 1 Appendix 2 Appendix 3 References Decision letter Author response Article and author information Metrics Abstract Although seasonality is widespread and can cause fluctuations in the intensity and direction of natural selection, we have little information about the consequences of seasonal fitness trade-offs for population dynamics. Here we exposed populations of Drosophila melanogaster to repeated seasonal changes in resources across 58 generations and used experimental and mathematical approaches to investigate how viability selection on body size in the non-breeding season could affect demography. We show that opposing seasonal episodes of natural selection on body size interacted with both direct and delayed density dependence to cause populations to undergo predictable multigenerational density cycles. Our results provide evidence that seasonality can set the conditions for life-history trade-offs and density dependence, which can, in turn, interact to cause multigenerational population cycles. https://doi.org/10.7554/eLife.18770.001 eLife digest Many wild populations go through long cycles in abundance that span several generations. The traditional explanation for such "multigenerational" cycles is that they are driven by predator/prey relationships, the classic example being oscillations between the numbers of lynx and snowshoe hares. Population cycles could also be driven by seasonal changes. For example, traits that help animals to produce large numbers of offspring during the breeding season may reduce the ability of the animal to survive the non-breeding season. Body size is one such trait. Large individuals tend to produce more offspring, but their larger body size means that they find it harder to survive when food is scarce. As a consequence, large individuals should have an advantage and be more common when the population size is low and there are enough resources for all individuals. However, small individuals should be more abundant when population size is high. This trade-off caused by seasonality could set the population in motion towards predictable, multigenerational cycles. To test this idea, Betini et al. established populations of fruit flies that went through 'breeding' and 'non-breeding' seasons. This was achieved by periodically altering the flies' food to prevent the females from laying eggs (in the lab, fruit flies do not normally have non-breeding seasons). Over 58 generations, the number of flies in each population cycled between peaks of high and low numbers. When the population contained relatively few flies, there was strong selection for large flies because they have high reproductive success. Hence, the population grew. When the population was large, meaning that the flies had to compete for a limited amount of food, there was strong selection for small flies because they are better able to survive on limited resources. However, small flies also produce fewer offspring on average, resulting in a decrease in population size. When the flies all had sufficient food during the non-breeding season, these regular cycles completely disappeared. A major challenge will be to understand how common this phenomenon is in the wild. Virtually all organisms live in seasonal environments but whether they face strong trade-offs in the expression of traits is not well understood. This is primarily because of the difficulty in following individuals throughout the year. https://doi.org/10.7554/eLife.18770.002 Introduction In many organisms, reproduction is confined to seasonal fluctuation in periods of high resource, in which both fecundity (reproduction) and viability (survival) selection can occur, and periods of low resources, when reproduction stops and natural selection occurs only through viability selection. Consequently, sequential episodes of reproduction and survival caused by seasonality could be a major source of fluctuations in the strength and direction of natural selection (Darwin, 1859; Lack, 1954; Fretwell, 1972; Schluter et al., 1991; Bell, 2010; Bergland et al., 2014), giving rise to classic life-history trade-offs (Lack, 1947; Roff, 1992; Stearns, 1992; Garland, 2014). More specifically, traits that confer a fecundity advantage, but which are associated with a survival cost, will experience natural selection in one season that is opposed by selection in the subsequent season (Levins, 1968; Michod, 2006; Bell, 2010; Bergland et al., 2014). The sequential rather than simultaneous nature of trade-offs driven by seasonality could have important consequence for the trait distribution within and across generations (Levins, 1968; Grafen, 1988; Michod, 2006) and population dynamics (Ozgul et al., 2010). One way by which life history trade-offs might arise from seasonal variation in resources is via body size (Ozgul et al., 2010, 2014). Large individuals usually have higher fecundity (Mueller and Joshi, 2000; Schulte-Hostedde and Millar, 2004), but they could also have lower survival during the non-breeding season when resources are scarce (Stockhoff, 1991; Reznick et al., 2000; Munch et al., 2003; Monaghan, 2008). In addition, large individuals might take more time to grow and require more resources for maintenance (Munch et al., 2003), which could negatively impact their survival probability (Kingsolver and Huey, 2008). This association between fitness and body size in seasonal environments could have important consequences for population dynamics, particularly when selection on body size is density-dependent (Mueller, 1997; Sinervo et al., 2000; Travis et al., 2013). Differences in the selective advantage of body size across seasons could also shed light on the long-standing question about why population densities of many species fluctuate periodically over time (Elton and Nicholson, 1942; Kendall et al., 1999; McCauley et al., 2008; Yan et al., 2013). For example, when body size is positively related to fecundity, but small individuals survive better in the non-breeding season (Stockhoff, 1991; Munch et al., 2003; Monaghan, 2008; Betini et al., 2014), these opposing patterns of selection could cause population cycles if selection is density-dependent. Specifically, if smaller offspring have higher survival when density is high, then the population will be composed of smaller than average individuals with lower average fecundity in the following breeding season. This lower mean fecundity will reduce population growth rates even though larger individuals will be favoured through fecundity selection. As population size declines, the strength of density-dependent viability selection on body size will also decline, which could cause net selection to reverse and favour larger individuals due to the fecundity benefit of being larger. As large individuals increase in frequency, population size should also increase via an improvement of reproductive output, returning populations to high densities. Although changes in the intensity and direction of natural selection caused by environmental variation are widespread (Schluter et al., 1991; Bell, 2010; Thompson, 2013; Bergland et al., 2014), we have little information about whether opposing episodes of natural selection could arise from seasonality and indirectly affect population dynamics through the feedback loop between ecological (density dependence) and evolutionary (selection and evolution) processes (Chitty, 1960; Krebs, 1978; Hairston et al., 2005; Pelletier et al., 2009; Ozgul et al., 2010; Schoener, 2011). Here, we investigated how a seasonal fitness trade-off related to body-size could affect changes in population size and body size over time using replicate populations of Drosophila melanogaster exposed to repeated changes in food resources. In addition to standard breeding conditions for Drosophila, we also created a 'non-breeding season' by manipulating the food medium to prevent females from laying eggs during this period. Thus, in this system, breeding and survival were restricted to two sequential and distinct seasons (hereafter 'breeding' and 'non-breeding'). The number of days and amount of food in each season was determined so that both fecundity and non-breeding survival were density-dependent (Betini et al., 2013a, 2014, 2015), which is an important feature of many populations. In Drosophila, as in many other species, the positive correlation between body size and fecundity is well known (Mueller and Joshi, 2000; Appendix 1) and we previously demonstrated that small individuals have higher survival during the non-breeding season when abundance is high (Betini et al. 2013a, 2014). In addition, populations of D. melanogaster do not show evidence of multigenerational cycles (Mueller and Joshi, 2000), even when kept under the same conditions as our breeding season (i.e. 'aseasonal populations'; Appendix 2). We, therefore, hypothesized that density dependence and opposing episodes of fecundity and viability selection on body resulting from seasonality could cause predictable and repeatable fluctuations in both population and body size. Specifically, we predicted that seasonal fitness trade-offs would cause population size and body size to undergo multigenerational cycles between periods of high abundance, when small individuals predominate, and periods of low abundance, when large individuals are more frequent. Furthermore, we predicted that populations not exposed to viability selection in the non-breeding season would lack periodic fluctuations in population size and body size. We tested whether seasonality could result in multigenerational cycles in population size and body size using three experiments (Figure 1). In the first experiment, we submitted 45 replicate populations to the seasonal treatment described above and tracked the total number of individuals and body size at the end of the breeding and non-breeding season for 58 generations (the 'long-term control' treatment; Figure 1). In the second experiment, we tested the role of viability selection during the non-breeding season by tracking 13 additional populations over 31 generations using a similar protocol to the 'long-term control', but in which we experimentally prevented viability selection in the 'non-breeding' season by providing high levels of food during this season (the 'stop-selection' treatment; Figure 1). This protocol also maintained direct density effects on fecundity and survival, similar to the ones observed in the 'long-term control'. In order to address potential environmental changes in the lab, we conducted a third experiment using the same protocol as in the 'long-term control', but under the same initial conditions and at the same time as the 'stop selection' treatment. This 'short-term control' experiment also had 13 replicate populations tracked over 31 generations (Figure 1). Figure 1 Download asset Open asset A schematic of the three experiments conducted in this study with accompanying duration, number of replicates and brief summary of their purpose. https://doi.org/10.7554/eLife.18770.003 In addition to these experiments, we also developed a mathematical model to investigate the contributions of both viability selection and delayed density dependence to population dynamics. The 'stop-selection' experiment was designed to eliminate viability selection, but might have also reduced potential effects of past densities on fecundity and survival. Such delayed density-dependent effects can also cause populations to cycle (Stenseth et al., 2003; Yan et al., 2013), or lead to more complex dynamics, such as chaos (May 1973). One potential mechanism for delayed density dependence are carry-over effects, which we have previously identified in this seasonal system (Betini et al., 2013a). Thus, we first investigated if lag effects were present in all three experiments, and then used the mathematical model to understand whether they played a role in the dynamics of their populations. Results Long-term control Over 58 generations, the 45 replicated seasonal populations showed a predictable increase in abundance during the breeding season, where the food medium allowed females to lay eggs, and a decline in the subsequent non-breeding season (Figure 2a), as is typical of many natural seasonal systems. However, the autocorrelation functions (ACF) also revealed that these short, seasonal cycles were embedded within longer multigenerational cycles where average population size fluctuated 3-fold (insert in Figure 2a). In these populations, the ACF function was characterized by stationary periodic dynamics, which resulted in an oscillatory decay to zero (Figure 2a inset). Figure 2 Download asset Open asset Population size, changes in body size and selection differentials for body size in the 'long-term control' experiment. (a) Population size of seasonal flies cycled over 58 generations; (b) Female dry weight before (blue bars) and after (black bars) the non-breeding season. Vertical bars indicate the mean female dry weight before and after the non-breeding season; (c) Increased population size in the non-breeding season led to stronger directional selection for smaller flies. (d) Time series of female dry weight measured at the end of the non-breeding season over 38 generations. In (a and (d), the autocorrelograms (insets) showed evidence of cycles in both population size and body size. In (a solid blue line denotes mean population size for each generation from all replicates and dotted lines denote ±1 s.d. In (d, the horizontal line within each box represents the median value, the edges are 25th and 75th percentiles, the whiskers extend to the most extreme data points, and points are potential outliers. https://doi.org/10.7554/eLife.18770.004 To investigate the presence of viability selection for small body size and whether this selection was density-dependent, we measured female dry weight in 38 generations from 25 different populations. As expected, there is a negative correlation between population size at the end of the non-breeding season and body size at the end of the non-breeding season (Pearson's product-moment correlation = −0.64; t = −4.48, p<0.001), suggesting that density negatively impact body size in the non-breeding season. Mean survival during the non-breeding season was 71% (±0.21 SD) and survival was density-dependent (βsurvival = −0.001, t = −27.73, p<0.001). Mean female dry weight was significantly lower after the non-breeding season (0.279 mg, n = 3620 females) than before the non-breeding season (0.381 mg; n = 5258 females; standardized values = 0.577 before and −0.566 after the non-breeding season; Welch t-test: t = −35.90, df = 1,589.240.24, p<0.001; Figure 2b) and this viability selection was density-dependent (Figure 2c; Table 1, Appendix 3). That is, when population size was high at the start of the non-breeding season, there was stronger selection for smaller flies and this was driven by changes in mean dry weight after the non-breeding season rather than changes in the mean dry weight before the non-breeding season (Appendix 3). Average dry weight measured after the non-breeding season also showed multigenerational cycles (Figure 2d), as indicated by the autocorrelation function (Figure 2d, inset), varying between average peaks of 0.32 mg and lows of 0.23 mg. Table 1 Parameter estimates obtained from linear mixed effect models to investigate viability selection on body size as a function of thenumber of individuals at the beginning of the non-breeding season. In the 'long-term control', R2LMM(m)=0.18 and R2LMM(c)=0.20; in the 'stop selection' treatment, R2LMM(m)=0.006 and R2LMM(c)=0.006; and in the 'short-term control', R2LMM(m)=0.22 and R2LMM(c)=0.22. R2LMM(m) is the variance on the response variable that is explained only by the fixed effects and R2LMM(c) is the variance that is explained by both fixed and random effects. In all models, the selection differential was the response variable, abundance at the beginning of the non-breeding season was the fixed effect and population (vial) was the random effect. https://doi.org/10.7554/eLife.18770.005 Parameters Fixed effects estimate SE Df T P 1. Long-term control Intercept −0.181 0.081434.5−2.22 0.027Non-breeding abundance −0.004 0.003745.3−12.67 <0.001 2. Stop selection Intercept −0.341 0.159159−2.15 0.033Non-breeding abundance 0.0010.0011591.060.2913. Short-term control Intercept 0.0280.184100−0.15 0.880Non-breeding abundance −0.005 0.001139−6.44 <0.001 'Stop selection' experiment In order to test the role of viability selection in these multigenerational cycles, we experimentally eliminated viability selection during the non-breeding season in 13 additional populations. Unlike the 'long-term controls' (Figure 2a), there was no evidence of multigenerational population cycles in these 'stop selection' populations (Figure 3a inset). In addition, body size did not significantly decline after the non-breeding season (Figure 3b; average body size was 0.337 mg before and 0.331 after the non-breeding season; n = 1290 and n = 689 females, respectively; standardized values: 0.028 before and −0.052, respectively; Welch t-test: t = −1.733, df = 1,479.400.40, p=0.081). There was also no evidence of density-dependent selection (Figure 3c; Table 1) and no evidence of cycles in body size (Figure 3d inset). Figure 3 Download asset Open asset Population size, changes in body size and selection differential for body size in the 'stop-selection' experiment. (a) Population size of seasonal flies cycled over 31 generations. Unlike the 'long-term control, (b) there was no significant change in body size after the non-breeding season (female dry weight before - red bars - and after -black bars- the non-breeding season; vertical bars indicates the mean female dry weight before and after the non-breeding season) and (c) no evidence that selection for smaller flies was density dependence. (d) Time series of female dry weight measured at the end of the non-breeding season over 27 generations. In (a) and (d), the autocorrelograms (insets) showed no evidence of cycles in population or body size. In a solid red line denotes the mean population size for each generation from all replicates and dotted lines denote ±1 s.d. In (d), the horizontal line within each box represents the median value, the edges are 25th and 75th percentiles, the whiskers extend to the most extreme data points, and points are potential outliers. https://doi.org/10.7554/eLife.18770.006 'Short-term control' Over 31 generations, and similar to the 'long-term control' (Figure 2a), the 'short-term control' exhibited evidence for multigenerational cycles (Figure 4a). These 'short-term control' populations also experienced viability selection that was density-dependent. Overall, female dry weight significantly decreased from an average of 0.371 mg before the non-breeding season (n = 968 females) to 0.276 mg after the non-breeding season (n = 623 females; standardized values = 0.487 before and −0.761 after the non-breeding season; Welch t-test: t = −30.601, p<0.001; Figure 4b), but the magnitude of this viability selection was stronger when densities were higher at the start of the non-breeding season (Table 1, Figure 4c). Figure 4 Download asset Open asset Population size, changes in body size and selection differentials for body size in the 'short-term control' experiment. (a) Population size of seasonal flies cycled over 31 generations, as suggested by the autocorrelogram (insets), (b) female dry weight before the non-breeding season (blue bars) was higher than after the non-breeding season (red bars; vertical bars indicate the mean female dry weight before and after the non-breeding season). (c) increased population size in the non-breeding season led to stronger directional selection for smaller flies. In (a) solid black line denotes mean population size for each generation from all replicates and dotted lines denote ±1 s.d. In (d, the horizontal line within each box represents the median value, the edges are 25th and 75th percentiles, the whiskers extend to the most extreme data points, and points are potential outliers. https://doi.org/10.7554/eLife.18770.007 Delayed density dependence We statistically investigated whether fecundity and survival were influenced by density in past seasons (i.e. delayed density dependence) in all three experiments: 'long-term control', 'short-term control' and 'stop-selection'. We used linear mixed effect models with vial (population) as a random effect and densities going back up to two generations as fixed effects. In the 'long-term control' and 'short-term control', fecundity and survival were influenced by density in the current and past season (Table 2 and Table 3). In contrast, the 'stop-selection' experiment showed evidence of the delayed effects on fecundity (Table 2), but not on survival (Table 3), meaning that the 'stop-selection' treatment eliminated both viability selection on body size as well as delayed effects of density on survival. Table 2 Parameter estimates obtained from linear mixed effect models to investigate the effects of current and past density on fecundity in the 'long-term control', 'stop-selection' and 'short-term control' experiments. B refers to population size at the beginning of the breeding season in the current season and NB refers to population size at the beginning of the previous non-breeding season. In the 'long-term control', R2LMM(m)=0.34 and R2LMM(c)=0.37; in the 'stop selection' treatment, R2LMM(m)=0.07 and R2LMM(c)=0.07; and in the 'short-term control', R2LMM(m)=0.30 and R2LMM(c)=0.30. https://doi.org/10.7554/eLife.18770.008 Parameters Fixed effects estimate SE T P 1. Long-term control Intercept 0.4500.01237.445<0.001 B −0.212 0.008−25.82 <0.001 NB −0.008 0.008−1.05 0.296B * NB 0.0260.0055.07<0.001 2. Stop-selection Intercept 0.5510.02422.91<0.001 B 0.1500.0532.820.005NB −0.156 0.034−4.53 <0.001 B * NB 0.06130.032.310.0212. Short-term control Intercept 0.5320.01927.72<0.001 B −0.226 0.024−9.34 <0.001 NB −0.039 0.022−1.74 0.083B * NB 0.0460.0172.650.008 Table 3 Parameter estimates obtained from linear mixed effect models to investigate the effects of current and past density on survival in the 'long-term control', 'stop-selection' and 'short-term control' experiments. NB refers to population size at the beginning of the non-breeding season in the current generation. B1, NB1, B2 and NB2, refers the population size at the beginning of each season going back 1 or two generations, respectively. In the 'long-term control', R2LMM(m)=0.35 and R2LMM(c)=0.36; in the 'stop selection' treatment, R2LMM(m)=0.99 and R2LMM(c)=0.99; and in the 'short-term control', R2LMM(m)=0.43 and R2LMM(c)=0.43. https://doi.org/10.7554/eLife.18770.009 Parameters Fixed effects estimate SE T P 1. Long-term control Intercept −0.353 0.006−54.74 <0.001 NB −0.186 0.006−31.19 <0.001 B1 0.1060.00813.76<0.001 NB1 −0.056 0.007−8.34 <0.001 B2 0.0440.0075.67<0.001 NB2 −0.020 0.007−2.89 0.0042. Stop-selection Intercept −0.489 0.001−1,068.62<0.001 NB −0.213 0.001−412.71 <0.001 B1 0.0010.0011.3250.186NB1 −0.001 0.001−1.235 0.217B2 0.0010.0010.4790.632NB2 0.0010.0010.2250.8223. Short-term control Intercept −0.427 0.013−33.36 <0.001 NB −0.223 0.0142−15.64 <0.001 B1 0.1440.0157.22<0.001 NB1 −0.037 0.015−2.40 0.017B2 0.0410.0202.030.043NB2 −0.015 0.016−0.933 0.351 Mathematical model A mathematical model including delayed density dependence as well as the effects of body size on survival (viability selection) and fecundity resulted in multigenerational cycles in population size (before red line in Figure 5a), similar to those observed in our 'long-term control' and 'short-term control' (Figure 2a and Figure 4a, respectively). The model without viability selection on body size and delayed density dependence (i.e. including only effects of current abundance on fecundity and survival), resulted in the elimination of multigenerational cycles (after red line in Figure 5a), as observed in our 'stop selection' populations (Figure 3a). The exclusion of only viability selection eliminated the fitness trade-off in body size and allowed larger flies to survive to breed. This led to unstable population dynamics (i.e. the population crashed after 10 generations; Figure 5b) because larger flies have greater fecundity and there was a negative interaction between body size and abundance. The exclusion of delayed density dependence alone eliminated the cycles (Figure 5c), suggesting that viability selection and delayed density dependence are necessary for these persistent multigenerational cycles to occur. The model with low heritability (h2 = 10−5) also generated multigenerational population cycles (Figure 5d). Figure 5 Download asset Open asset Predicted population size according to the integral Time series generated with the model (a) for the first generations (before vertical red when both viability selection and delayed density effects on survival during the non-breeding season and fecundity were for the generations, only the effects of current population size on fecundity and survival were (i.e. no viability selection and no delayed density (b) population size the effects of viability selection the effects of delayed density dependence on fecundity and survival were or (c) the effects of delayed density dependence the effects of viability selection were In (d), series were generated as in (a) but with low heritability Results for In population crashed (i.e. population size at generation In both (b) and the model the effects of current abundance on fecundity and survival and heritability for body size. In (a) and (d) autocorrelograms for population size obtained from the mathematical model including delayed density dependence, viability and fecundity selection (before red or without both delayed density dependence and viability selection (after red and methods for and model Discussion Our results provide and mathematical evidence that the between and evolutionary trade-offs caused by seasonality can have important consequences for population dynamics. In our experimental system, seasonal variation in resources resulted in a fitness trade-off and multigenerational population cycles. These cycles were observed in the of fluctuations in resources, or dependence, all of which are known to cause regular fluctuations in population size et al., Yan et al., 2013). Thus, the of population cycles caused by three common of natural populations a life-history trade-off and that these ecological and evolutionary processes could to fluctuations in population size over a of and environments than previously Our experimental elimination of viability selection and delayed and our mathematical model the of both of these evolutionary and ecological processes in the of multigenerational population cycles resulting from seasonal it that dynamics are for oscillations in population size et al., 2005; et al., 2014), but evidence for evolutionary change (i.e. change in to feedback and and population dynamics is but et al., 2013). Our results that the evolutionary response to selection might not be to feedback between ecological and evolutionary as long as selection is In flies, as in many other species, body size is and and it is to in our populations, offspring from smaller flies tend to be However, even when variation is strong selection can affect trait within generations population size. In our experimental system, selection for body size during the non-breeding season was strong enough to observed cycles, in the of change across generations. with our mathematical model with zero heritability (h2 = as opposed to also generated multigenerational population cycles because viability selection the distribution of body size, which Thus, changes in the trait distribution within a generation caused by seasonal fitness trade-offs could feedback between ecological and evolutionary in traits across generations. We showed that variation in non-breeding abundance can cause

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