Two larval foraging strategies in Drosophila have been identified, 'rover' and 'sitter'. 'Rovers' traverse a large area while feeding whereas 'sitters' cover a small area. The difference between 'rovers' and 'sitters' was analyzed genetically by chromosomal substitutions between isogenic stocks. Differences in larval locomotor behavior ('crawling behavior') can be attributed to the second chromosome, the 'rover' strategy being dominant over the 'sitter' strategy. Differences in feeding rate ('shoveling behavior') are affected additively by both the second and third chromosomes. Natural populations of Drosophila larvae were sampled three times over a 2-month period' 'rovers' and 'sitters' were at constant frequencies in these populations. The two foraging strategies are discussed in the light of resource utilization in environments where food is distributed continuously or discontinuously (Sokolowski, 1980).
Localizing genes for quantitative traits by conventional recombination mapping is a formidable challenge because environmental variation, minor genes, and genetic markers have modifying effects on continuously varying phenotypes. The method of 'lethal tagging' is described; it was used in conjunction with deficiency mapping for localizing major genes associated with quantitative traits. Rover/sitter is a naturally occurring larval foraging polymorphism in Drosophila that has a polygenic pattern of inheritance comprised of a single major gene (foraging) and minor modifier genes. The lethal tagged foraging (for) gene has been successfully localized by deficiency mapping to 24A3-C5 on the polytene chromosome map (de Belle, 1989).
There is a correlation between the locomotory component of larval and adult foraging behavior in the fruit fly. This relationship is far more than mere correlation. It can be attributable to different alleles at the same genetic locus of the behavioral gene foraging (for). The for gene offers an unique opportunity to study the genetic basis and evolutionary significance of a naturally occurring behavioral polymorphism. Until now, only the effect of for on Drosophila larval behavior was studied. Larvae with the rover allele (forR) move significantly more while eating during a set time period than those homozygous for the sitter alleles (fors). Rover and sitter larval strains derived from nature differ in the distance adults walk after feeding per unit time and this variation results from different alleles at the foraging locus, the very gene originally defined on the basis of larval behavior. It is hypothesized that for may be involved in the way flies evaluate a food resource (Pereira, 1993).
The ability of larvae and adult rover and sitter flies to detect and migrate towards the source of a fly medium attractant was investigated using larval plate assays and an adult olfactory trap assay. Allelic variation at the foraging locus does not affect larval olfactory response in the larval plate assays. In contrast, adult males of the sitter mutant fors2 exhibit an olfactory trap response (OTR) which is significantly greater than that of males of the wild type forR strain from which fors2 was derived and further genetic analysis shows that this is attributable to the fors2 allele. The olfactory responses of fbrR and fors2 flies to three odors (propionic acid, ethyl acetate and acetone) in a T-maze assay is normal, indicating that they do not have general olfactory deficits. The finding that adult flies who differ in their PKG enzyme activities differ in foraging behaviors and olfactory trap responses to yeast odors, suggests that PKG signalling pathways are involved in olfactory related responses to food (Shaver, 1998).
Natural variation in neuronal excitability and connectivity has not been extensively studied. In Drosophila, a naturally maintained genetic polymorphism at a cGMP-dependent protein kinase (PKG) gene, foraging, is associated with alternative food search strategies among the allelic variants Rover (forR; higher PKG activity) and sitter (fors; lower PKG activity). Physiological and morphological variations were examined in nervous systems of these allelic variants isolated from natural populations. Whole-cell current clamping revealed distinct excitability patterns, with spontaneous activities and excessive evoked firing in cultured sitter, but not Rover, neurons. Voltage-clamp examination demonstrated reduced voltage-dependent K(+) currents in sitter neurons. Focal recordings from synapses at the larval neuromuscular junction demonstrate spontaneous activity and supernumerary discharges with increased transmitter release after nerve stimulation. Immunolabeling show more diffuse motor axon terminal projections with increased ectopic nerve entry points in sitter larval muscles. The differences between the two natural alleles were enhanced in laboratory-induced mutant alleles of the for gene. The pervasive effects of the for-PKG on neuronal excitability, synaptic transmission, and nerve connectivity illustrate the magnitude of neuronal variability in Drosophila that can be attributed to a single gene. These findings establish the consequences in cellular function for natural variation in an isoform of PKG and suggest a role for natural selection in maintaining variation in neuronal properties (Renger, 1999).
The cGMP-dependent protein kinase (PKG) has many cellular functions in vertebrates and insects that affect complex behaviors such as locomotion and foraging. The foraging (for) gene encodes a PKG in Drosophila melanogaster. A function for the for gene in sensory responsiveness and nonassociative learning has been demonstrated. Larvae of the natural variant sitter (fors) show less locomotor activity during feeding and have a lower PKG activity than rover (forR) larvae. rover and sitter adult flies were used to test whether PKG activity affects (1) responsiveness to sucrose stimuli applied to the front tarsi, and (2) habituation of proboscis extension after repeated sucrose stimulation. To determine whether the differences observed resulted from variation in the for gene, fors2, a sitter mutant produced on a rover genetic background was tested. Rovers (forR) are more responsive to sucrose than sitters (fors and fors2) at 1-, 2-, and 3-wk old. This is true for both sexes. Differences in sucrose responsiveness between rovers and sitters are greater after 2 h of food deprivation than after 24 h. Of flies with similar sucrose responsiveness, forR rovers showed less habituation and generalization of habituation than fors and fors2 sitters. These results show that PKG independently affects sensory responsiveness and habituation in Drosophila melanogaster (Scheiner, 2004).
One of the rare examples of a single major gene underlying a naturally occurring behavioral polymorphism is the foraging locus of Drosophila. Larvae with the rover allele, forR, have significantly longer foraging path lengths on a yeast paste than do those homozygous for the sitter allele, fors. These variants do not differ in general activity in the absence of food. The evolutionary significance of this polymorphism is not as yet understood. The effect of high and low animal rearing densities on the larval foraging path-length phenotype has been examined; density-dependent natural selection produces changes in this trait. In three unrelated base populations the long path (rover) phenotype was selected for under high-density rearing conditions, whereas the short path (sitter) phenotype was selected for under low-density conditions. Genetic crosses suggested that these changes resulted from alterations in the frequency of the fors allele in the low-density-selected lines. Further experiments showed that density-dependent selection during the larval stage rather than the adult stage of development is sufficient to explain these results. Density-dependent mechanisms may be sufficient to maintain variation in rover and sitter behavior in laboratory populations (Sokolowski, 1997).
Morphological polymorphisms have been shown to be affected by density-dependent selection in, for example, aphids, damsel flies, and ungulates. However, the importance of genetically based behavioral polymorphisms for population regulation has rarely been investigated. Populations of wild house mice, Mus musculus domesticus, exhibit two heritable alternative strategies called 'aggressive or active copers' and 'nonaggressive or passive copers'. 'Active copers' have a fitness advantage in established (called K type strategist) populations, whereas 'passive copers' are better at establishing new populations (called r type strategist) (Benus, 1991). In the current study, the rover phenotype was selected under high-density (K type) conditions, whereas the sitter was selected under low-density (r type) conditions. Both studies show a clear relationship between individual behavior and population dynamics (density- dependent selection). This study is the first to show a genetic basis to this relationship. One theoretical framework that these studies contribute to is the Chitty hypothesis (also called the self-regulation or the genetic control hypothesis) for population regulation that is based on the idea that populations can be regulated by factors intrinsic to the organism. In this scenario, directional selection is thought to act on behavioral morphs in a density-dependent manner such that the gene pool changes with population size. Thus, as in the present study, behavioral morphs are differentially selected under high (K-selected) as compared with low (r-selected) population densities. Although foraging behavior has been studied in detail by behavioral ecologists, little is known about the heritable basis of this trait and under what conditions individual differences in foraging behavior contribute to fitness. Two exceptions to this are the rover/sitter polymorphism investigated in this study and the foraging behavior of zebra finches (Taeniopygia guttato), which show heritable differences in the ability to discriminate between patches of food that differ in quality (Sokolowski, 1997 and references therein).
In the current study, density-dependent selection in the laboratory resulted in differences in larval foraging behavior in three independent experiments using three unrelated base populations. Low-density conditions selected for significantly shorter paths (sitter phenotype) in the m, mr, and UU lines and longer paths (rover phenotype) in the K, mK, and CU lines. The differences in behavior between the UU and CU lines suggested that density-dependent selection is important during the larval stages of development. Results of genetic crosses between the mr and mK lines and a strain carrying a deficiency of for demonstrated that some of the differences in behavior are attributable to variation at the for locus. The present study is of particular interest because it involves natural selection in the laboratory and not artificial selection. No artificial selection pressure on larval path length was placed on the high- and low-density treatment lines. The differences in path length resulted from high- compared with low-density rearing conditions, and these conditions constituted the selection pressure (Sokolowski, 1997).
It is difficult to make a case for the direct action of selection on a trait. Indeed, a number of factors could be responsible for density-dependent selection on larval path length. High-density compared with low-density cultures would differ in, for example, the distribution and concentration of food, waste products, and abiotic factors such as the moisture content of the medium. Larval density in the medium is an important biotic factor that varies in time and space. It is low during the early stages of medium infestation but higher during later stages. Variation in larval density also occurs within and between fruits (Sokolowski, 1997).
Drosophila larvae spend most of their lives foraging for food. They move through the food by extending their anterior end and retracting their posterior ends. They feed by shovelling the food (yeast) with their mouth hooks. In the absence of food, both rover and sitter larvae have long paths that do not differ from each other. Within a patch of food rover larvae exhibit significantly longer foraging trails than sitters. When food has a patchy distribution, rover larvae forage for food by moving between patches, whereas sitters forage within a patch. At high densities, larvae are required to crawl around other larvae, drowned pupae, and adults to reach a nearby food patch. In contrast, under low-density conditions, increased locomotory behavior (rover behavior) is unnecessary, since food is continuously distributed and of relatively higher quantity and quality. Thus patch size, patch quality, and interpatch distance would differ in high-density compared with low-density cultures. Indeed, the energetic cost of locomotion in Drosophila larvae is extremely high. In addition, larvae may be forced to look elsewhere for food under high-density conditions when food is limited. These factors should influence the success of rover compared with sitter larval behavior in high-density compared with low-density conditions (Sokolowski, 1997).
Density-dependent selection has been shown to influence a number of traits in Drosophila populations. Larval crowding increases pupation height (the distance larvae pupate from the food in vials) and larval feeding rate. The for gene does not have pleiotropic effects on these traits, although phenotypic correlations between larval path length and pupation behavior have been found in natural populations. Pupation height and larval feeding rate are polygenic characters influenced by many genes with additive effects on the major autosomes in Drosophila. From the perspective of larval fitness, feeding and moving are two of the most important behaviors performed in the larval period. Both larval behaviors (feeding rate and locomotion while foraging) show a significant response to density-dependent selection from larval crowding. Indeed, K lines evolved increased larval viability at high densities relative to the r lines (Sokolowski, 1997).
Density-dependent selection on the frequency of the rover and sitter phenotypes is a mechanism that could act both in the field and in the laboratory. In the laboratory, density-dependent selection likely arises from fly rearing methods. In the laboratory, 50-100 flies are placed in a bottle with culture medium, where they mate and lay eggs. Eggs are laid on the surface of the medium for several weeks. The larval period lasts 4-5 days at 25°C. The first larvae to hatch will experience low larval density conditions in contrast to larvae that hatch later. Thus larval density is low in the initial stages but high in the later stages of culture growth. Surveys of laboratory and natural populations have shown that some are polymorphic for rover/sitter behavior. Population numbers and larval density of D. melanogaster in the field also fluctuate both temporally (e.g., over the season) and spatially (between fruits). Indeed, population numbers may fluctuate dramatically as a consequence of density-dependent regulating mechanisms (Sokolowski, 1997 and references therein).
It should be possible to determine whether density-dependent selection affects the rover/sitter polymorphism in field populations because this polymorphism is found as a single gene (for). However, performing behavioral assays for rover/sitter phenotypic frequencies in the field is a difficult task. This is because the character being measured is a behavioral one and phenotypic frequencies will not always be representative of the true underlying genotypic frequencies due to, for example, incomplete penetrance. Proper aging of the larva and strict control of environmental conditions (i.e., food availability) are important for minimizing the probability of misclassifying a rover as a sitter or vice versa. These types of controls are impossible to implement in the field. Thus DNA probes are being developed for rover and sitter alleles to assess their frequencies in the field. These probes can then be used to address the density-dependent selection hypothesis in a variety of natural populations whose density varies temporally and/or spatially. Experimental manipulations of population densities in the field along with careful monitoring of the polymorphism should enable a furthering of understanding of how density-dependent selection contributes to the maintenance of the rover/sitter polymorphism (Sokolowski, 1997).
Fluid transport in Drosophila tubules is regulated by guanosine 3',5'-cyclic monophosphate (cGMP) signalling. The functional effects on tubules of different alleles of the foraging gene were compared; the fors allele confers an epithelial phenotype. This manifests itself as hypersensitivity of epithelial fluid transport to the nitridergic neuropeptide, capa-1, which acts through nitric oxide and cGMP. However, there was no significant difference in tubule cGK activity between fors and forR adults. Nonetheless, fors tubules contained higher levels of cGMP-specific phosphodiesterase (cG-PDE) activity compared to forR. This increase in cGMP-PDE activity suffices to decrease cGMP content in fors tubules compared to forR. Challenge of tubules with capa-1 increases cGMP content in both fors and forR tubules, although the increase from resting cGMP levels is greater in fors tubules. Capa-1 stimulation of tubules reveals a potent inhibition of cGMP-specific phosphodiesterase in both lines, although this is greater in fors; and is sufficient to explain the hypersensitive transport phenotype observed. Thus, polymorphisms at the for locus do indeed confer a cGMP-dependent transport phenotype, but this can best be ascribed to an indirect modulation of cGMP-specific phosphodiesterase activity, and thence cGMP homeostasis, rather than a direct effect on cGK levels (MacPherson, 2004).
Animals must be able to find and evaluate food to ensure survival. The ability to associate a cue with the presence of food is advantageous because it allows an animal to quickly identify a situation associated with a good, bad, or even harmful food. Identifying genes underlying these natural learned responses is essential to understanding this ability. This study investigated whether natural variation in the foraging (for) gene in Drosophila larvae is important in mediating associations between either an odor or a light stimulus and food reward. It was found that for influences olfactory conditioning and that the mushroom bodies play a role in this for-mediated olfactory learning. Genotypes associated with high activity of the product of for, cGMP-dependent protein kinase (PKG), showed greater memory acquisition and retention compared with genotypes associated with low activity of PKG when trained with three conditioning trials. Interestingly, increasing the number of training trials resulted in decreased memory retention only in genotypes associated with high PKG activity. The difference in the dynamics of memory acquisition and retention between variants of for suggests that the ability to learn and retain an association may be linked to the foraging strategies of the two variants (Kaun, 2007).
While many studies have suggested the importance of cAMP signaling in associative learning, the current results implicate the cGMP signaling pathway in mediating reward learning and memory. Specifically, the results suggest a novel role for the foraging gene in larval learning and memory. for plays a more robust role in larval olfactory reward conditioning than larval visual reward conditioning. It was also found that the role of for in larval olfactory reward conditioning involves the mushroom bodies. These results suggest that the role of for in olfactory memory is dependent on training experience, suggesting that for may be involved in multiple mechanisms that influence formation of olfactory associations. The evidence suggests that these mechanisms affect the training experience necessary for memory acquisition and retention. For example, fors (the sitter variants) larvae respond to an increase in the number of training trials compared with forR (the rover variants) larvae. Interestingly, for also plays a role in short- and long-term memory in Drosophila adults, suggesting that these mechanisms may be conserved throughout development (Kaun, 2007).
for may also play a role in the mechanisms that affect the time-course of training necessary to produce memory acquisition and retention. The results suggest that increased PKG activity is associated with faster learning, and decreased PKG activity is associated with slower learning. As mentioned above, these differences may be related to the alternative foraging strategies of forR and fors larvae. forR larvae move more when foraging, and thus, potentially come across many food patches, whereas sitters move less and potentially stay close to a smaller number of food patches. Thus, it may be advantageous for forR larvae to quickly form an association between a new food source and odor and then use this new information to assess the quality of future food sources. Decreased memory retention may be advantageous for rovers, as previous studies suggest that formation and retention of formed associations can be energetically costly. Conversely, staying longer in a single food patch may result in a delay in the ability to form an association between a food source and odor in fors larvae. However, it may aid in the ability of fors larvae to remember which nearby food patches had been depleted (Kaun, 2007).
Intriguingly, rover adult flies show a slower rate of habituation compared with sitter adult flies upon repetitive presentation of stimuli. forR flies show less habituation and generalization of habituation to repeated sucrose stimuli compared with fors and fors2 flies. This is consistent with a more rapid response decrement of the giant-fiber escape circuit in fors and fors2 flies compared with forR flies as measured electrophysiologically. Since repetitive stimuli in the form of odor-reward pairings are used in the current study, the decrease in LI seen after increasing the amount of odor-reward pairings may, in part, represent a response decrement to the stimuli (Kaun, 2007).
The differences in olfactory learning and memory due to for may be inextricably linked to the different foraging strategies of the two natural variants. This leads to the question of whether for may play a role in other behaviors associated with foraging and food such as path-integration, territoriality, aggression, and courtship. If so, for may play a role in higher-order reward pathways that mediate these individual behaviors. Interestingly, the mushroom bodies play a role in such complex behaviors, including courtship, courtship conditioning, spatial learning, aggression, and sleep. Accordingly, the role of the mushroom bodies in for-dependent larval reward learning hints at a role of for in more complex behaviors involving higher-order reward pathways. Future research will provide insight as to whether a role of for in a variety of complex behaviors exists (Kaun, 2007).
Knowing which genes contribute to natural variation in learning and memory would help in the understanding of how differences in these cognitive traits evolve among populations and species. A natural polymorphism at the foraging (for) locus, which encodes a cGMP-dependent protein kinase (PKG), affects associative olfactory learning in Drosophila melanogaster. In an assay that tests the ability to associate an odor with mechanical shock, flies homozygous for one natural allelic variant of this gene (forR) showed better short-term but poorer long-term memory than flies homozygous for another natural allele (fors). The fors allele is characterized by reduced PKG activity. forR-like levels of both short-term learning and long-term memory can be induced in fors flies by selectively increasing the level of PKG in the mushroom bodies, which are centers of olfactory learning in the fly brain. Thus, the natural polymorphism at for may mediate an evolutionary tradeoff between short- and long-term memory. The respective strengths of learning performance of the two genotypes seem coadapted with their effects on foraging behavior: forR flies move more between food patches and so could particularly benefit from fast learning, whereas fors flies are more sedentary, which should favor good long-term memory (Mery, 2007b).
The cellular functions of PKG are poorly elucidated, and its downstream effectors, for the most part, are unknown. Mammalian PKG (also called cGKI) plays a role in synaptic plasticity (long-term potentiation and depression) and seems to act both pre- and postsynaptically as a downstream component of nitric oxide signaling. Mice deficient in cGKI are defective in a cerebellum-dependent motor-learning task (Feil, 2003), but their performance in hippocampus-dependent learning is apparently not affected (Kleppisch, 2003). However, pharmacological potentiation of NO-cGMP signaling was reported to improve the performance of mice in a hippocampus-dependent learning task, the water maze (Chien, 2005), whereas pharmacological inhibition of PKG impaired memory retrieval in chickens (Edwards, 2002). Finally, NO-cGMP signaling was recently shown to interact with a cAMP-dependent mechanism in long-term memory formation in crickets (Matsumoto, 2006). Although pharmacological inhibition of PKG had no effect on memory in that study, it indicated that memory processes dependent on cGMP may run in parallel to processes mediated by other signaling pathways, like the rut adenylate cyclase-dependent memory trace (Mery, 2007b).
Interactions between such parallel pathways might be responsible for the antagonistic effects of for-PKG on short- and long-term memory, which are reported here. Yet, long-term memory is thought to form on the basis of short-term memory (with middle-term memory being an intermediate step), so one would rather expect them to be positively correlated. A positive correlation between short-term learning performance and long-term memory was observed in fly populations subject to selection for improved performance in an ecologically relevant oviposition learning task (Mery, 2007a). The antagonistic effects of FOR on short-term learning performance and long-term memory reported here are thus unexpected and call for more research on the role of cGMP-dependent processed in memory formation (Mery, 2007b).
Although the mechanism by which for-PKG acts to modulate learning and memory are unknown, these findings clearly point to mushroom bodies as the spatial focus of its action. FOR expressed in all three subsets of mushroom body neurons (α/β, α'/β', and γ). However, transgenic expression of forT2 transcript restricted to the α/β neurons was sufficient to induce forR-like pattern of short- and long-term memory in fors flies. The α/β neurons play a central role in olfactory memory: memory retrieval relies on synaptic output from these neurons, and the α lobes contain a long-term memory trace. However, a role of FOR in α'/β' and γ neurons, which have also been implicated in olfactory learning, cannot be excluded. In particular, the GAL4 driver 201Y shows only weak expression in the α/β neurons and apparently only in those that project to the cores of the α/β lobes; this line seems to express more strongly in the γ neurons. Yet, using it to drive the expression of forT2 had the same effect on learning performance as that using the other two driver lines. This implies either that a low level of forT2 expression in the α/β neurons is sufficient for the full effect on short- and long-term memory, or that forT2 expression in the γ neurons also contributes to this effect. Identification of GAL4 lines specific to α'/β' and γ neurons will help to resolve the effect of for expression in those neurons on memory formation and consolidation (Mery, 2007b).
There is a wealth of evidence for the ecological significance of learning in a variety of insects. In Drosophila, experimental data suggest that larvae use learning to find food and avoid predators; oviposition substrate choice of females is modified by experience; and males learn to discriminate against heterospecific females and to recognize unreceptive females of their own species, as well as refine their courtship behavior. Thus, even though the understanding of ecological aspects of learning in fruit flies is still rudimentary, there is evidence that it contributes to their fitness under natural conditions. This would explain why Drosophila are capable of learning, despite learning ability being a costly adaptation. But is the effect of for polymorphism on learning and memory ecologically relevant? The classical conditioning paradigm used in this paper allows control of the amount of shock and odors received by the flies and dissection of the memory dynamics, but its relevance to situations in which Drosophila learn in nature is unclear. Nonetheless, different forms of olfactory learning, involving different contexts and stimuli, rely at least in part on the same genes and neural circuits and are affected by the same naturally occurring genetic variation. In accord with that notion, the for alleles also affect larval appetitive learning. Thus, it is reasonable to expect that the learning and memory differences among for genotypes will affect their learning performance in nature and thus may contribute to natural selection on this polymorphism (Mery, 2007b).
The extent to which learning ability is favored by natural selection and which aspects are favored should depend on the environment. In particular, fast learning would be highly advantageous if the environment changed frequently within the lifetime of an individual, whereas good long-term memory would be particularly useful in more stable environments. Arguably, rover (forR) flies are more prone to encounter different environments within their lifetime than sitter (fors) flies; they spend less time feeding at one location, both as larvae and as adults, and are more likely to leave a patch of food in search of another one. It is thus tempting to speculate that the superior short-term learning performance of forR flies and the good long-term memory of fors flies form elements of complex rover and sitter evolutionary strategies, respectively adapted to variable and constant environments. However, one might also argue that rover flies would benefit from good long-term memory if they revisit places visited previously; resolving this argument would require a better understanding of Drosophila field ecology than currently is currently available. In the absence of evidence, it is more parsimonious to regard the antagonistic effects of the for alleles on short-term learning and long-term memory as a mechanistic consequence of the role of PKG in neuronal processes. As discussed above, too little is known about this role to understand the mechanism of this antagonism. It is also not clear whether this antagonism is typical for natural allelic variants, leading to a strong tradeoff between short- and long-term memory. The pattern of genetic correlations among different memory phases in natural gene pools has not been investigated, except for one study (Mery, 2007a) where both short-term learning rate and long-term memory improved in response to selection on learning performance in an ecologically relevant task (Mery, 2007b).
Whether they form part of coadapted alternative strategies or are mechanistic consequences of differences in PKG activity, the learning and long-term memory differences among for genotypes are likely to contribute to natural selection on the allelic variants of for polymorphism. However, in addition to its effect on learning, the for polymorphism influences a number of other behavioral and physiological traits of ecological relevance. It also affects larval competitive ability in a density-dependent manner, whereby high population density favors the forR allele and low density favors the fors allele. Furthermore, under some circumstances, negative frequency-dependent selection seems to favor whichever of the two alleles is currently rare, likely contributing to the maintenance of this polymorphism in nature. Thus, the overall force of selection acting on the for alleles will reflect the aggregate impact of their manifold pleiotropic effects on survival and reproduction. If such a high degree of pleiotropy were typical of natural alleles affecting learning, there would be two important consequences for evolution of cognitive traits. First, evolutionary changes in learning ability would be associated with changes in other ecologically relevant traits. Second, improved learning or memory might evolve as a byproduct of natural selection on other traits rather than because of fitness advantages of learning itself (Mery, 2007b).
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