Density-dependent selection at low food levels leads to the evolution of population stability in Drosophila melanogaster even without an inverse r-K relationship

Population stability ultimately depends on the life-history characteristics of individuals; thus, it may be indirectly affected by natural selection acting on various life-history traits. This study investigates the efficacy of natural selection in molding the stability of populations living at an unstable equilibrium. The stability of laboratory populations of Drosophila is affected by the relative amount of food given to larvae and adults. Environments with high larval food levels and low adult food levels (HL environments) tend to have asymptotically stable carrying capacities. Environments with low larval food levels and high adult food levels (LH environments) tend to exhibit unstable dynamics, like population cycles. In this experiment, 20 populations were created from two different types of source populations. Five of the source populations had evolved for 71 generations under crowded larval conditions and uncrowded adult conditions (CU populations), while the other five source populations had evolved for a comparable time in uncrowded larval and uncrowded adult conditions (UU). In this study, five replicate CU and UU populations each were placed in both the HL and LH environments, and total adult population counts and adult biomass were recorded for 45 generations. Every five generations, we also estimated the density-dependent fecundity function in each population, since population stability depends critically on the shape of this function. While we could document phenotypic evolution in these populations for several characters due to density-dependent natural selection, there was no detectable change in the population stability characteristics of the unstable LH populations. This result is consistent with either no evolution of population stability, or very slow change. Thus, while evolution in these populations affects important life-history characteristics, these changes appear to have no detectable effects on population stability.

Theories of density-dependent natural selection predict that evolution should favor those genotypes with the highest per capita rates of population growth under the current density conditions. These theories are silent about the mechanisms that may give rise to these increases in density-dependent growth rates. We have observed the evolution of six populations of Drosophila melanogaster recently placed in crowded environments after nearly 200 generations at low-population density in the laboratory. After 25 generations in these crowded cultures all six populations showed the predicted increase in population growth rates at high-population density with the concomitant decrease in their growth rates at low densities. These changes in rates of population growth are accompanied by changes in the feeding and pupation behavior of the larvae: those populations that have evolved at high-population densities have higher feeding rates and are less likely to pupate on or near the food surface than populations maintained at low densities. These changes in behavior serve to increase the competitive ability of larvae for limited food and reduce mortality under crowded conditions during the pupal stage of development. A detailed understanding of the mechanisms by which populations evolve under density-dependent natural selection will provide a framework for understanding the nature of trade-offs in life history evolution.

The effects of adult crowding on two components of fitness were studied in three sets of Drosophila melanogaster populations, subjected to life-stage-specific, density-dependent natural selection in the laboratory for over 50 generations. Three days of crowding, early in adult life, were observed to increase mortality significantly during the episode of crowding, as well as decrease subsequent fecundity. Populations selected for adaptation to high adult densities suffered significantly lower mortality during episodes of adult crowding, as compared to populations selected specifically for adaptation to larval crowding, as well as control populations typically maintained at low larval and adult densities. Moreover, populations adapted to larval crowding seemed to be adversely affected by adult crowding to a greater extent than the controls, raising the possibility of trade-offs between adaptations to larval and adult crowding, respectively. Preliminary evidence suggests that the populations adapted to adult crowding may have evolved a propensity to stay away from the food medium, which is where most deaths occur when adults are crowded in culture vials.

Density-dependent selection is expected to lead to population stability, especially if r and K tradeoff. Yet, there is no empirical evidence of adaptation to crowding leading to the evolution of stability. We show that populations of Drosophila ananassae selected for adaptation to larval crowding have higher K and lower r, and evolve greater stability than controls. We also show that increased population growth rates at high density can enhance stability, even in the absence of a decrease in r, by ensuring that the crowding adapted populations do not fall to very low sizes. We discuss our results in the context of traits known to have diverged between the selected and control populations, and compare our results with previous work on the evolution of stability in D. melanogaster. Overall, our results suggest that density-dependent selection may be an important factor promoting the evolution of relatively stable dynamics in natural populations.

Article Figures and data Abstract eLife digest Introduction Results Discussion Materials and methods References Decision letter Author response Article and author information Metrics Abstract How the nervous system internally represents environmental food availability is poorly understood. Here, we show that quantitative information about food abundance is encoded by combinatorial neuron-specific gene-expression of conserved TGFβ and serotonin pathway components in Caenorhabditis elegans. Crosstalk and auto-regulation between these pathways alters the shape, dynamic range, and population variance of the gene-expression responses of daf-7 (TGFβ) and tph-1 (tryptophan hydroxylase) to food availability. These intricate regulatory features provide distinct mechanisms for TGFβ and serotonin signaling to tune the accuracy of this multi-neuron code: daf-7 primarily regulates gene-expression variability, while tph-1 primarily regulates the dynamic range of gene-expression responses. This code is functional because daf-7 and tph-1 mutations bidirectionally attenuate food level-dependent changes in lifespan. Our results reveal a neural code for food abundance and demonstrate that gene expression serves as an additional layer of information processing in the nervous system to control long-term physiology. https://doi.org/10.7554/eLife.06259.001 eLife digest To maximize their chances of survival, animals need to be able to sense changes in the abundance of food in their environment and respond in an appropriate manner. The nervous system is able to sense cues from the environment and coordinate responses in the whole organism, but it is not clear how this leads to long-term changes in the organism's biology. In nematode worms, two genes called daf-7 and tph-1 appear to be involved in connecting the sensing of food availability with changes in the biology of the organism. The daf-7 gene encodes a hormone, while tph-1 encodes an enzyme that makes a neurochemical called serotonin. Here, Entchev, Patel, Zhan et al. found that daf-7 and tph-1 genes are active in three pairs of neurons in nematode worms. The experiments show that these neurons collectively form a circuit that carries information about the abundance of food, which leads to changes in how long the worms live. When this circuit was disrupted by removing these genes, the worms' ability to adjust their lifespan in response to changes in the availability of food was weakened, likely because they were unable to sense food. The experiments also show that the circuit regulates itself, largely because daf-7 and tph-1 are able to control each-other's activity. Together, these results suggest that changing the activity of certain genes in neurons enables nematode worms to alter their biology in response to changes in the availability of food. Neurons in the brain use electrical activity to communicate and process information and Entchev, Patel, Zhan et al.'s findings imply that gene activity can also perform a similar role. https://doi.org/10.7554/eLife.06259.002 Introduction All organisms need to accurately assess their environment to respond to changes that impact their survival. Environmental changes such as food availability can lead to alterations in organismal physiology, such as stress resistance and metabolic states that have consequences for clinically important outputs such as disease progression, health, fecundity and lifespan (Libert and Pletcher, 2007). Many conserved genetic mechanisms that govern these alterations to physiology have been identified (Libert and Pletcher, 2007; Berthoud and Morrison, 2008; Rother et al., 2008; Alcedo et al., 2010; Koch and Horvath, 2014). Yet, how these genetic pathways encode and process information about the environment to elicit physiological outputs in vivo is unclear at a quantitative and mechanistic level, despite their importance for health and disease. In animals, the nervous system is the central site for processing sensory information and coordinates organism-wide responses to changing conditions. Food availability is a critical environmental variable that modulates metabolism and other physiological outputs via neuroendocrine circuits (Berthoud and Morrison, 2008; Rother et al., 2008; Alcedo et al., 2010; Koch and Horvath, 2014). In contrast to well-studied sensory modalities such as vision and olfaction (Baier, 2013; Wilson, 2013), where neural processing occurs on short timescales using electrical signals, how food availability is internally represented across a broad range of inputs to regulate long-term, food-related physiological responses remains virtually unknown. A particularly interesting food-related response is the role of dietary restriction (DR) in modulating lifespan in diverse species (Bishop and Guarente, 2007; Mair and Dillin, 2008; Fontana et al., 2010; Alic and Partridge, 2011). DR occurs through changes that likely happen over long timescales (hours to days), unlike fast behavioral responses to visual or olfactory cues. Neural gene expression also occurs over long timescales (minutes to hours) and is thus well suited for functionally encoding food abundance during DR. In Caenorhabditis elegans, daf-7 and tph-1 are conserved components of neural TGFβ and serotonin signaling pathways, respectively, and are associated with food sensing and modulation of organismal physiology. daf-7 encodes a TGFβ family member (Ren et al., 1996), while tph-1 encodes tryptophan hydroxylase, the rate-limiting enzyme for serotonin synthesis (Sze et al., 2000). In C. elegans, TGFβ and serotonin signaling affect lifespan and metabolism, consistent with conserved roles from invertebrates to mammals (Sze et al., 2000; Ashrafi, 2007; Murakami and Murakami, 2007; Petrascheck et al., 2007; Shaw et al., 2007; Brown and Schneyer, 2010; Oury and Karsenty, 2011). tph-1 and daf-7 are expressed in an environmentally responsive manner in specific neurons with food-related functions (Ren et al., 1996; Schackwitz et al., 1996; Sze et al., 2000; Zhang et al., 2005; Chang et al., 2006; Liang et al., 2006; Greer et al., 2008; Pocock and Hobert, 2010). daf-7 is expressed in the ASI sensory neurons, whose activities are responsive to bacterial food (Ren et al., 1996; Gallagher et al., 2013; Zaslaver et al., 2015). Starvation reduces daf-7 expression in ASI, and laser ablations of ASI extend lifespan, consistent with the role of daf-7 and other ASI-expressed genes in modulating lifespan (Ren et al., 1996; Alcedo and Kenyon, 2004; Bishop and Guarente, 2007). tph-1 is expressed in the NSM foregut neurons, the ADF sensory neurons, and the HSN motorneurons involved in egg-laying (Sze et al., 2000). Both serotonin signaling mutants and NSM ablation affect food-modulated locomotion, consistent with the idea that serotonin from NSM acts in this food-related response (Sawin et al., 2000). In the food-responsive ADF neurons (Zaslaver et al., 2015), tph-1 expression is responsive to pathogenic bacteria and starvation, to respectively mediate aversive olfactory plasticity and stress responses (Zhang et al., 2005; Liang et al., 2006). daf-7 and tph-1 are therefore strong candidates for mediating the link between environmental cues and longevity. Nonetheless, how these genes cooperate to quantitatively encode a broad range of food levels to modulate lifespan is unknown. Gene-expression responses to food cues have largely been studied as ON/OFF switches to the presence or absence of food (Zinke et al., 2002; Baugh et al., 2009). Because food abundance is a continuous variable, we sought to understand how expression of tph-1 and daf-7 could allow animals to distinguish multiple food levels. Furthermore, gene expression is inherently variable (Eldar and Elowitz, 2010), but this property is rarely studied in vivo in multicellular animals; thus we also sought to determine how gene-expression variability affects the ability of the worm to encode its environment. Here we show that daf-7 and tph-1 expression in three pairs of neurons forms a distributed circuit that quantitatively encodes food abundance and mediates dietary effects on lifespan in C. elegans. Specific disruptions to this circuit resulted in corresponding attenuation in the ability to discriminate between food levels in both the gene-expression code and lifespan output. We found that this circuit tunes its own accuracy, largely via the regulation of the dynamic range and variability of food-responsive gene expression by tph-1 and daf-7 signalling, respectively. Our work suggests that neural regulation of gene expression in conserved pathways can couple environmental sensation to physiological output, and highlights a novel mechanism for information processing by the nervous system to impact physiology. Results Two neuronal genes mediate bidirectional effects of DR on lifespan During DR, lifespan increases as food levels are decreased from ad libitum conditions until reaching a maximum, beyond which further food reduction lowers lifespan (Bishop and Guarente, 2007; Mair and Dillin, 2008; Fontana et al., 2010; Alic and Partridge, 2011). To fully understand the response to food levels that C. elegans might encounter in the wild (Felix and Duveau, 2012), we modified a well-established DR protocol (Greer et al., 2007) (Figure 1A) to measure the lifespans of wildtype animals shifted as day 2 adults to 19 concentrations of the Escherichia coli food source across ∼11 orders of magnitude (Figure 1B, Figure 1—figure supplement 1 and Figure 1—source data 1). We inhibited progeny production with egg-5(RNAi) (Figure 1A) to prevent matricide due to internal hatching at low food levels. This treatment does not affect the lifespan response to food; similar responses were observed in wildtype animals without egg-5(RNAi) (Figure 1—figure supplement 1), and are found in the literature where similar subsets of food ranges were tested using other DR protocols (below). Figure 1 with 2 supplements see all Download asset Open asset Two neuronal genes, daf-7 and tph-1, shape a complex, multiphasic relationship between lifespan and food availability. (A) Protocol for maintaining animals at different food levels for lifespan and imaging experiments. Effects of initiating different dietary restriction (DR) on different days are shown in Figure 1—figure supplement 1A,B. (B) Mean lifespan of wildtype worms subjected to 19 food levels ranging from 0–3.5 × 1010 bacterial cells/ml at 20°C. Points denoting key features in the food response and used as food conditions in subsequent experiments are highlighted. Figure 1—figure supplement 1D shows that these lifespan responses have similar shapes across different temperatures. The lifespan data are shown in Figure 1—source data 1. (C) Mean lifespans of wildtype and mutant animals across the six food levels indicated in (B) show that loss of tph-1 and daf-7 preserves the pattern but attenuates the range of the lifespan response. Genotypes are indicated by the legends below (E) and (F). The lifespan data are shown in Figure 1—source data 2, and statistical comparisons between the different genotypes and food levels are shown in Figure 1—source data 3. (D) tph-1 and daf-7 modulation of lifespan is bidirectional and their epistatic relationship is food-specific. The epistatic interaction between the two genes in the tph-1(−); daf-7(−) double mutant differs depending on food level. The double mutant resembled the tph-1(−) single mutant in the absence of a bacterial food source and resembled the daf-7(−) single mutant at a high bacterial food concentration. (E) Range of food-induced lifespan modulation for each genotype. Range is defined by the difference between the highest and lowest mean lifespan response across the six food levels. (F) Average of the mean lifespan responses across all food levels for each genotype reveals a consistent, food-independent baseline lifespan response. The schedule for transferring animals to different conditions in these lifespans are shown in Figure 1—figure supplement 2. https://doi.org/10.7554/eLife.06259.003 Figure 1—source data 1 Summary of wild type lifespan outputs under the full range of food levels tested. https://doi.org/10.7554/eLife.06259.004 Download elife-06259-fig1-data1-v1.xlsx Figure 1—source data 2 Summary of wild type and mutant lifespan outputs under six selected food levels. https://doi.org/10.7554/eLife.06259.005 Download elife-06259-fig1-data2-v1.xlsx Figure 1—source data 3 Statistical significance of lifespan modulation across food levels and genetic backgrounds. https://doi.org/10.7554/eLife.06259.006 Download elife-06259-fig1-data3-v1.xlsx We uncovered a multiphasic relationship between bacterial abundance and longevity that is more complex than previously reported with smaller concentration ranges (Figure 1B) (Greer et al., 2007; Greer and Brunet, 2009; Ching et al., 2010). We found that lifespan increased and then decreased as bacterial concentration was reduced from the highest level, forming a DR response consistent with prior reports at high food ranges (Bishop and Guarente, 2007; Panowski et al., 2007; Greer and Brunet, 2009; Mair et al., 2009; Ching et al., 2010). Surprisingly, upon further reduction, lifespan increased again till a plateau was reached, suggesting that the initial decrease was not due to limiting nutrients. The longest lifespans occurred in the absence of bacteria, where the magnitudes of these effects were consistent with published dietary deprivation experiments (Kaeberlein et al., 2006; Lee et al., 2006). This relationship between lifespan and food abundance was maintained across temperatures (Figure 1—figure supplement 1), suggesting a robust food-sensing process. This multiphasic food response may reflect trade-offs between multiple food-regulated processes as previously discussed (Kaeberlein et al., 2006; Lee et al., 2006). Here we used the complex lifespan response as a functional basis for understanding how neuronal gene expression could encode food abundance. To understand how the multiphasic lifespan response to food abundance is regulated, we measured the lifespan of daf-7 and tph-1 null mutants across six bacterial concentrations that captured the complexity of broad-range DR (circled in Figure 1B). Prior studies suggested that daf-7 and tph-1 mediate lifespan extension (Murakami and Murakami, 2007; Shaw et al., 2007; van der Goot et al., 2012). We showed that their effects were in fact bidirectional: these genes could either extend or reduce lifespan in a food-specific manner (Figure 1C, Figure 1—source data 2, 3). Both single mutants had reduced lifespans at low food levels and increased lifespan at 6 × 108 cells/ml in comparison to wildtype; additionally, daf-7(−) mutants were long-lived at the highest food level (Figure 1C). The magnitude of lifespan changes we observed at high food levels (1 × 1010 cells/ml) were comparable to prior studies performed at ad libitum food conditions (Murakami and Murakami, 2007; Shaw et al., 2007). Intriguingly, tph-1 and daf-7 influenced the longevity response more strongly at low and high bacterial concentrations respectively (Figure 1D), suggesting that they act at different but overlapping ranges of food. Furthermore, the double mutant resembled the tph-1(−) mutant at low bacterial levels and the daf-7(−) mutant at high bacterial levels (Figure 1D), suggesting that these genes act in parallel rather than in a linear pathway. Together, these phenotypes indicate that daf-7(−) and tph-1(−) mutants were neither intrinsically long- nor short-lived; instead, their phenotypes and genetic interactions were modulated by extensive gene-environment interactions. Rather than altering the basic pattern of the lifespan response to food, loss of tph-1 or daf-7, either alone or in combination, dampened food responsiveness by bidirectionally attenuating extension and reduction of lifespan due to DR (Figure 1C,D). This effect was manifested in the diminished range of lifespans across all food levels in both the daf-7(−) and tph-1(−) single mutants, which was further reduced in the double mutant (Figure 1E). This result also supports the idea that these genes act in parallel pathways. Furthermore, the mean lifespan across all food levels were similar in all the genotypes tested (Figure 1F), suggesting that mutations in tph-1 and daf-7 lowered the food-responsive component of longevity around a consistent, food-independent lifespan that may be specified by other environmental parameters such as temperature (Figure 1E and Figure 1—figure supplement 1). This bidirectional dampening of the food response and preservation of an underlying lifespan differs from previously described DR regulators, such as aak-2, daf-16, pha-4 and skn-1, whose mutants abolish DR-mediated lifespan extension (Bishop and Guarente, 2007; Greer et al., 2007; Panowski et al., 2007). Thus, tph-1 and daf-7 mutants reveal a previously unobserved DR phenotype, and our results suggest that these genes mediate a bidirectional lifespan response to DR. Neuronal expression of daf-7 and tph-1 encodes food abundance tph-1 is expressed in the ADF sensory neurons, the NSM neurons within the foregut, and the hermaphrodite-specific HSN motor neurons (Sze et al., 2000). daf-7 is expressed in a single pair of ASI sensory neurons (Ren et al., 1996; Schackwitz et al., 1996). To determine whether tph-1 and daf-7 act in these neurons to modulate lifespan, we expressed these genes in specific neurons and tested their ability to rescue the lifespan phenotypes in the tph-1(−); daf-7(−) double mutant. Expression of tph-1 in either ADF or NSM neurons (Figure 2A–C) or of daf-7 in ASI neurons (Figure 2D,E) could rescue the lifespan phenotypes at low and high food levels, respectively. These results indicate that the activity of tph-1 and daf-7 in these respective neurons are relevant to lifespan modulation. Figure 2 Download asset Open asset Neuron-specific rescue of lifespan phenotypes. (A) Lifespan outcomes of wildtype, tph-1(−) and daf-7(−) single mutants and the tph-1(−); daf-7(−) double mutant indicates that the double mutant closely resembles the tph-1(−) mutant in the absence of a bacterial food source. (B) In the absence of bacterial food, restoration of tph-1 activity in the NSM neurons via the expression of a tph-1 cDNA driven by the ceh-2 promoter rescues the lifespan reduction observed in the tph-1(−); daf-7(−) double mutants. (C) Restoration of tph-1 expression in the ADF neurons via the srh-142 promoter also shows reversal of the lifespan reduction. (D) Lifespan outcomes of wildtype, tph-1(−) and daf-7(−) single mutants and the tph-1(−); daf-7(−) double mutant indicates that the double mutant closely resembles the daf-7(−) mutant at a high concentration of the bacterial food source. (E) At high food level, restoration of daf-7 expression in the ASI neurons via the expression of daf-7 under the gpa-4 promoter reverses the lifespan extension observed in the tph-1(−); daf-7(−) double mutants. All comparisons are drawn against non-transgenic siblings of animals bearing the extrachromosomal array of interest. https://doi.org/10.7554/eLife.06259.009 Previous studies showed that daf-7 and tph-1 expression are regulated by environmental cues (Ren et al., 1996; Schackwitz et al., 1996; Sze et al., 2000; Zhang et al., 2005; Chang et al., 2006; Liang et al., 2006; Greer et al., 2008; Pocock and Hobert, 2010). However, their expression profiles over a broad range of inputs remain unknown because manual studies limit the number of animals and environmental conditions that can be feasibly studied in a consistent way. To overcome these limitations, we used an automated, high-throughput microfluidic-based platform (Figure 3A and Figure 3—figure supplement 1) (Chung et al., 2008; Crane et al., 2012) for quantitative large-scale imaging of individual worms bearing single-copy fluorescent transcriptional reporters for both tph-1 and daf-7 (Ptph-1::mCherry and Pdaf-7::Venus) across different food levels (Figure 3B). For brevity, we refer to these reporter activities as tph-1 and daf-7 expression. Our reporters contain the same regulatory regions as published reporters that have been well validated, and show identical expression patterns (Ren et al., 1996; Schackwitz et al., 1996; Sze et al., 2000; Zhang et al., 2005; Chang et al., 2006; Liang et al., 2006; Greer et al., 2008; Pocock and Hobert, 2010) (Figure 3B). Starvation, hypoxia, or pathogenic bacteria alter both tph-1 reporter expression and serotonin levels (Zhang et al., 2005; Liang et al., 2006; Pocock and Hobert, 2010), while corresponding changes occur in daf-7 RNA levels and daf-7 reporter expression (Ren et al., 1996). These published results indicate that tph-1 and daf-7 reporters are faithful readouts for the expression of their respective genes (see ‘Materials and methods’ for additional details on reporter validation). Figure 3 with 1 supplement see all Download asset Open asset High-throughput quantitative imaging of tph-1 and daf-7 fluorescent reporters reveals neuron-specific, graded expression responses to food level. (A) Microfluidic system enabling high-throughput, neuron-specific quantitative imaging of gene expression in a large number of individual animals. Animals are transferred from culture plates to a liquid suspension at day 6 of adulthood and then loaded into the device for imaging. Figure 3—figure supplement 1 shows an overview of this imaging system. (B) Representative merged fluorescent image of transgenic worm with red and green fluorescent reporters for tph-1 and daf-7 transcriptional activity. Shapes indicate locations and identities of specific neurons. (C) Mean expression profiles of tph-1 in NSM (Ptph-1NSM) and ADF (Ptph-1ADF), and daf-7 in ASI (Pdaf-7ASI) across six different food levels are neuron-specific and largely non-monotonic. Measurements are normalized to the highest mean expression response observed in each respective neuron; error bars are SEM. (D) Distribution of the expression responses of tph-1 in NSM and ADF and daf-7 in ASI at different food levels. Means are indicated by the solid lighter-shade lines behind the distributions. Dashed line denotes the highest mean expression for each neuron, which was used for normalization. https://doi.org/10.7554/eLife.06259.010 We measured tph-1 expression levels in both NSM and ADF, and daf-7 in ASI, in animals exposed to the same six food levels that define our complex DR response (Figure 3C). Remarkably, we found that each neuron type had a specific pattern of activity across the six food levels (Figure 3C). Even with respect to a single gene, tph-1, the expression response in NSM differed from that in ADF, suggesting non-redundant roles of NSM and ADF in encoding bacterial abundance. Consistent with low tph-1 expression in the absence of food (Figure 3C), serotonin levels were reduced in NSM and ADF after starvation (‘Materials and methods’ and Liang et al., 2006). Notably, the responses of tph-1 in NSM and daf-7 in ASI were non-monotonic, prohibiting unique representation of the food level using either of these readouts The dynamic range and variability of the three expression patterns also suggesting different the sensory from food in different neurons (Figure the of reporter for each neuron type shifted in a graded manner across the six bacterial concentrations (Figure that the expression of tph-1 and daf-7 could provide information about a continuous range of environmental inputs for individual animals. This graded response with pathways, such as signalling, that outputs with a number of where the population to changing environmental conditions by of from to 1996). gene expression may be used to internally environmental conditions and mediate long-term physiological outputs such as we to expression in individual neurons with lifespan across food levels. We found that the expression levels of the individual genes in each neuron alone were to either food inputs or lifespan outputs (Figure largely due to expression and lifespan responses 3C). However, encoding across multiple neurons can the by animals to use a combinatorial to internally environmental conditions with (Figure Figure Download asset Open asset The of all neuronal gene-expression readouts a unique internal representation of food levels. (A) between individual gene-expression profiles and the lifespan responses across the six food levels indicates that the individual readouts are to lifespan responses. (B) The of tph-1 in NSM (Ptph-1NSM) and ADF and daf-7 in ASI (Pdaf-7ASI) a encoding of both food inputs and lifespan (C) The ability of expression and lifespan readouts to respond to and food conditions can be by using the readouts of to the food conditions. The results can be represented by where the in each indicate the with which are for a food level. readouts result in high represented by a overlapping response profiles result in low represented by a (D) the of tph-1 and daf-7 readouts or in similar encoding to that of lifespan outputs in wildtype animals. To assess the accuracy of the internal representation of food levels on the graded combinatorial expression of tph-1 and daf-7 in wildtype animals, we a (Figure and the gene-expression we this to the food level that individual animals were exposed This into the of gene and thus both and variance to decreased between the from different food levels leads to increased accuracy (Figure We neuronal encoding with a to the population of expression data at each food level. We food on expression in and then to the food level to determine the accuracy of the gene-expression responses. The results were as the of each food the food for each population (Figure the expression were distinct across food levels, a was in a strongly (Figure the then the food level was and the in the were to the number of food conditions tested (Figure expression data from ADF or ASI we showed that each neuronal had (Figure When neuron pairs were and particularly all three neuron pairs were the accuracy (Figure This result suggests that non-redundant encoding by each neuron pair the accuracy of the this system was at the highest and lowest food levels, consistent with the and of C. elegans in the wild (Felix and Duveau, 2012). the bacterial level, 6 × 108 where we observed the lowest lifespan, also showed a the graded and encoding may allow certain food levels, the ability was also by in the responses. To determine the accuracy of gene expression was for modulating lifespan, we how accurately the lifespan could be used to the food level using a similar This is important because the accuracy of the for the accuracy in the internal the accuracy of both the representation and be that the representation carries information for the output. In this we whether lifespan could also be used to the food level by an using on the of our Remarkably, the accuracy of lifespan was similar to that of gene expression (Figure that

Maternal nutritional state determines the sensitivity of Daphnia magna offspring to short-term Fenvalerate exposure

The cladoceran Moina macrocopa was used as test animal to investigate the effects of ibuprofen concentrations (0, 0.45, 0.9, 1.8, 3.6, 7.2 and 14.4 mg·L-1) on its life table demographic parameters under low (0.5×106 cells·mL-1), medium (1.0×106 cells·mL-1), and high (2.0×106 cells·mL-1) densities of Scenedesmus obliquus. The results showed that at low and high food levels, ibuprofen concentration significantly affected the intrinsic rate of population increase and the life expectancy of M. macrocopa, respectively. At all the three food levels, however, ibuprofen concentration did not significantly affect the generation time, net and gross reproduction rate of M. macrocopa. Compared with the controls, the intrinsic rate of population increase of M. macrocopaexposed to ibuprofen at 0.45, 0.9, 3.6 and 14.4 mg·L-1 was significantly decreased at low food level. At high food level, the life expectancy at hatching of M. macrocopa exposed to ibuprofen at 3.6 and 14.4 mg·L-1 was significantly increased. The results indicated that at low food level, certain concentrations of ibuprofen had negative effect on the population growth of M. macrocopa, which disappeared at medium and high food levels. At high food level, ibuprofen had positive effect on the survival of M. macrocopa, which disappeared at low and medium food levels. The effects of ibuprofen concentration on demographic parameters of M. macrocopa were dependent on food levels.

Directional and Stabilizing Density-Dependent Natural Selection for Pupation Height in Drosophila melanogaster

We have examined stability at the carrying capacity for 25 genetically different populations of Drosophila melanogaster. In spite of their genetic heterogeneity, 20 of the populations yield stable equilibria and none have eigenvalues significantly greater than one. Computer simulations demonstrate how selection at the individual level may account for population stability (and, hence, that group selection is not necessary for the evolution of stability). Recent theoretical studies on density—dependent selection in random environments provide predictions consistent with our empirical findings.

Patterns of selection: stress resistance and energy storage in density-dependent populations of Drosophila melanogaster

Density-dependent natural selection and age-specific natural selection are important determinants of life-history evolution. A variety of laboratory populations of Drosophila melanogaster have been created to study the effects of these selection mechanisms. Two types of populations have been selected for reproduction early (B) and late (O) in life. These have exhibited changes in life span and resistance to stresses, such as desiccation, starvation, ethanol vapours and flying to exhaustion. Similarly, two types of populations have been selected at high adult and larval densities (K) and low adult and larval densities (r)

The theory of density-dependent natural selection predicts that populations kept at extreme densities should evolve different competitive abilities for limited resources. These predictions have been tested with laboratory populations of Drosophila melanogaster. Six independent populations were maintained in two environments, called r and K, for 128 generations. In the r environment, population sizes were small and resources for larvae and adults were abundant. In contrast the populations in the K environment were large and crowded, and resources, such as food and space, were in short supply. The relative competitive ability for food has been estimated for each population. Populations from the K environment consume food at a rate that is 58% greater than the average rate for the r population. The differentiation of competitive abilities in these populations is due to natural selection and is consistent with predictions from the theory of evolutionary ecology.

Summary Populations of Drosophila melanogaster kept at high population density (K-selected) for 125 generations have higher larval viability than populations kept at low densities (r-selected) when both are raised under crowded conditions. In addition K-selected adults that emerge from crowded cultures are larger than their r-selected counterparts. These differences cannot be explained by differences in efficiency of food use. The minimum food required for successful pupation is actually greater in the K-selected populations. I conjecture that there may be a trade-off between minimum food requirements and competitive ability, which has changed substantially in the K-selected populations. The possibility that K-selected larvae can dig more more deeply and gain access to unused food is examined and rejected as a possible explanation of the viability differences. Evidence is provided supporting the hypothesis that the differences in viability may be due to an increased tendency of the K-selected larvae to pupate off the surface of the medium.

Two Decades of Drosophila Population Dynamics: Modeling, Experiments, and Implications

Effect of food level on the growth and survival of laboratory-reared larvae of bay anchovy ( anchoa mitchilli Valenciennes) and scaled sardine ( harengula pensacolae Goode & Bean)