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Popul Ecol (2010) 52:5–14 DOI 10.1007/s10144-009-0187-8 SPECIAL FEATURE: REVIEW Rapid Adaptation Rapid adaptation: a new dimension for evolutionary perspectives in ecology Masakazu Shimada • Yumiko Ishii Harunobu Shibao • Received: 7 October 2009 / Accepted: 9 November 2009 / Published online: 5 December 2009 The Society of Population Ecology and Springer 2009 Abstract Although the study of adaptation is central to biology, two types of adaptation are recognized in the biological field: physiological adaptation (accommodation or acclimation; an individual organism’s phenotype is adjusted to its environment) and evolutionary–biological adaptation (adaptation is shaped by natural selection acting on genetic variation). The history of the former concept dates to the late nineteenth and early twentieth centuries, and has more recently been systemized in the twenty-first century. Approaches to the understanding of phenotypic plasticity and learning behavior have only recently been developed, based on cellular–histological and behavioral– neurobiological techniques as well as traditional molecular biology. New developments of the former concepts in phenotypic plasticity are discussed in bacterial persistence, wing di-/polymorphism with transgenerational effects, polyphenism in social insects, and defense traits for predator avoidance, including molecular biology analyses. We also discuss new studies on the concept of genetic accommodation resulting in evolution of phenotypic plasticity through a transgenerational change in the reaction norm based on a threshold model. Learning behavior can also be understood as physiological phenotypic plasticity, associating with the brain–nervous system, and it drives the accelerated evolutionary change in behavioral response (the Baldwin effect) with memory stock. Furthermore, choice behaviors are widely seen in decision-making of animal foragers. Incorporating flexible phenotypic plasticity and learning behavior into modeling can drastically change dynamical behavior of the system. Unification of M. Shimada (&) Y. Ishii H. Shibao Department of Systems Sciences, University of Tokyo, Komaba, Tokyo 153-8902, Japan e-mail: [email protected] biological sciences will be facilitated and integrated, such as behavioral ecology and behavioral neurobiology in the area of learning, and evolutionary ecology and molecular developmental biology in the theme of phenotypic plasticity. Keywords Behavioral neurobiology Choice behavior Genetic accommodation Memory and learning Phenotypic plasticity Predation switching Introduction: rapid adaptation in nature Two concepts of adaptation Bock (1980) stated that biological adaptation is a property of the phenotypic features of an organism relative to the selection demands of the environment. Adaptation promotes properties of form and function that enable the organism to survive in the environment. Although the study of adaptation is central to biology, there have been two interpretations of this concept. Futuyma (1986) noted that ‘‘In physiology, adaptation is often used to describe an individual organism’s phenotypic adjustment to its environment, as in physiological acclimation. In evolutionary biology, however, an adaptation is a feature that, because it increases fitness, has been shaped by specific forces of natural selection acting on genetic variation’’ (chap. 9, p. 251). In the latter concept, indeed, an emphasis on cost–benefit analysis of the individual fitness of traits has commonly been emphasized in research fields first established in the 1970s, including evolutionary ecology (MacArthur 1972; Pianka 1978; Ricklefs 1979), behavioral ecology (Krebs and Davies 1978; 1981; Sibly and Smith 1985), and 123 6 sociobiology (Wilson 1975). Such traditional evolutionary views originated from the mutation–selection concept in the synthetic theory of population genetics (see Fisher 1930). On the other hand, the former concept based on physiological and behavioral features of adaptation (including acclimation, phenotypic plasticity, learning, and epigenetics) is related to short-term, condition-dependent changes within a framework of genetic programming that is molded in much longer evolutionary time scales of at least dozens of generations. Although ‘acclimation’ and ‘accommodation’ have been widely recognized since the middle of the twentieth century, the phenotypic plasticity includes these classical concepts as a new terminology that has prevailed in studies of plants, animals, and even bacteria (Pigliucci 2001; West-Eberhard 2003; Kirshner and Gerhart 2005). We will show here the ubiquitous phenomena in nature. Ubiquitous phenomena of rapid adaptation in nature Polyphenism involving distinct morphologies has been extensively reported in insects, for example, the di-/polymorphism of wing formation (in aphids, plant hoppers, and locusts) and the cast differentiation of social insects (ants, bees, wasps, and termites) (West-Eberhard 1989). In addition, several prey–predator systems show inducible defense traits for predator avoidance, such as the tadpole and salamander system (Van Buskirk and Relyea 1998; Wilson et al. 2005; Kishida and Nishimura 2006; Kishida et al. 2006, 2009, 2010), and the Daphnia and predators (small fish or larval phantom midge Chaoborus) system (Levins 1968; Harvell 1990; Havel and Dodson 1984; Tollrian 1993; Tollrian and Dodson 1999; Hammill et al. 2008; Engel and Tollrian 2009). Molecular biology studies of the mechanisms of phenotypic plasticity have recently elucidated the conditional partial on/off switching of the promoter and/or enhancer region in gene expression (Gerhart and Kirshner 1997; Kirshner and Gerhart 1998, 2005). Furthermore, epigenetic traits (condition-dependent modification with methylation and acetylation in DNA and histone proteins) can be prolonged over several generations (Kalisz and Purugganan 2004). With respect to learning behavior, animals can lean from environmental cues during foraging; for example, marks and chemical kairomones enable predators to locate prey in their habitat. However, as learning into long-term memory has a cost (Mery and Kawecki 2005), the learning behavior of animals involves a cost–performance balance from both the evolutionary–ecological and behavioral–neurobiological points of view. Furthermore, a spreading effect of learning behavior can include the generation of complicated population dynamics involving predator switching 123 Popul Ecol (2010) 52:5–14 (Oaten and Murdoch 1975; Murdoch and Oaten 1975; Ishii and Shimada 2010). This is based on the trade-off of attention (‘limited attention’; Dukas and Kamil 2001; Dukas 2002, 2004), in which a predator’s attention to prey is formed through ‘conditioning’ to the most common prey in situations where multiple prey–predator systems occur in the habitat. Integrated understanding of learning behavior spreads from behavioral neurobiology to population dynamics and evolutionary ecology. The potential for rapid adaptation will be naturally selected through genetic variation on the basis of learning and phenotypic plasticity (Kawecki 2010), which will result in adaptive evolution at a longer time scale (the Baldwin effect; Mery and Kawecki 2004b; Crispo 2007; Paenke et al. 2007; Lande 2009). In recent decades, learning behaviors have gradually been elucidated through studies of behavioral neurobiology (Zupanc 2003), especially those involving prolonged memory storage through stimulus repetition (Kandel 2001). Incorporating such phenotypic plasticity and choice behaviors into prey–predator systems can greatly change a dynamical behavior of the system (Abrams 2010; Ishii and Shimada 2010). The aim of this review is to synthesize recent findings in research on phenotypic plasticity and learning behavior with reference to as many as possible molecular–cellular biology, physiology and genome science developments, and to propose a new dimension for evolutionary perspectives in ecology. Phenotypic plasticity in physiological and morphological adaptation Bacterial phenotypic plasticity Phenotypic plasticity occurs in prokaryotes as well as eukaryotes. The most famous example is the conditiondependent gene expression based on the bacterial operon, in which gene expression is clearly changed in response to nutritional conditions (Jacob and Monod 1961). For another example, the filament formation (elongation four or five times longer in the cell length) has been widely observed in Escherichia coli when they are cultivated under environmental stress, e.g., poor nutrient medium or high temperature (Maki et al. 2000). It is also recognized that response of bacteria to antibiotics in bacterial growth media enables bacterial persistence. Wakamoto et al. (2005), Wakamoto and Yasuda (2006a, b) and Ayano et al. (2006) reported that a proportion of successive Escherichia coli populations survived when antibiotics were provided at intermittent intervals. If resistance were a result of evolutionary change based on Popul Ecol (2010) 52:5–14 mutation–selection processes, the survival ratio would be higher in successive populations. However, the survival ratio was constant under the antibiotic regime; such bacterial survivorship patterns have been termed ‘persistence’, not resistance (Wakamoto et al. 2005; Wakamoto and Yasuda 2006a, b). Stochastic gene expression has been recognized here, whereby division and growth of daughter cells is unbalanced and asymmetric with respect to cell size and physiological properties (Blake et al. 2001; Furusawa and Kaneko 2001; Baetz and Kaern 2006; Kaneko 2007; Fraser and Kaern 2009). Wing dimorphism and polymorphism in insects Polyphenism involving distinct morphologies has been extensively reported in insects in wing dimorphism (brachyptera and macroptera); in the plant hopper (Homoptera) (Kishimoto 1956, 1976; Iwanaga et al. 1985, 1987; Iwanaga and Tojo 1986; Morooka and Tojo 1992), the aphid (Homoptera) (Dixon et al. 1993; Weisser et al. 1999; Braendle et al. 2006), the water strider (Heteroptera) (Vespäläinen 1978; Goodwyn and Fujisaki 2007), the bug (Heteroptera) (Fujisaki 1992), and the cricket (Orthoptera) (Roff 1986; Zera and Tiebel 1989; Zera et al. 1999; Zhao and Zera 2002). Wing dimorphism depends partly on the population density. The brachiptera morph of the brown plant hopper (Nilaparvata lugens) occurs at low population densities and has high reproductive ability, whereas the macroptera morph often emerges at high population density and has a life history specialized for dispersal (Kishimoto 1956; Morooka and Tojo 1992). The wing polymorphism in N. lugens depends partly on the geographic strain, and the emergence ratio of the macroptera morph of N. lugens varies among localities from Japan to southeast Asia (Iwanaga et al. 1985, 1987; Iwanaga and Tojo 1986; S. Morooka, unpublished data). Molecular genetic analysis in wing dimorphism/polymorphism has, however, not been conducted either in the plant hopper or in the aphids, although Zera and Zhao (2006) reported biochemical basis of trade-off between dispersal and reproduction in a wing-polymorphic cricket, G. firmus. Aphids are currently becoming an important model organism, and a large community has begun to develop genomic resources for A. pisum. Braendle et al. (2005, 2006) reported that the male polymorphism is controlled by a single locus on the X chromosome called aphicarus (api) in the pea aphid, Acyrthosiphon pisum. In aphids, males are haploid for the X chromosome, so one allele of api causes winged males and the other causes wingless males. Three api genotypes are seen in natural populations: clones homozygous for the api-winged allele that produce all winged males, clones homozygous for the 7 api-wingless allele that produce all wingless males, and clones heterozygous for api that produce winged and wingless males in equal proportions (Braendle et al. 2006). The genome of the pea aphid A. pisum is currently being sequenced at a certain consortium. Polyphenism in social insects Another widely reported example of polyphenism in social insects is that of caste differentiation (polyethism) into workers, soldiers, and queens (Wilson 1971, 1975; Hölldobler and Wilson 1990). Colony mates have mother– daughter relationships in hymenopterous insects (ants, bees, and wasps), and different morphs (soldiers and normal) are genetic clones in the Homoptera (aphids). Genetically closely related or clonal insects show various properties in terms of morphology and behavior. In social aphids, altruistic individuals termed soldiers perform colony defense, housekeeping, and gall repair (Shibao et al. 2010). As aphids reproduce parthenogenetically (thelytoky), all members of a genetic clone have identical genomes. Nevertheless, social aphids display adaptive caste polyphenism and short-term behavioral flexibility, which permits rapid responses to changing environmental and social stimuli. For example, in Tuberaphis styraci, which has a sterile soldier caste in the second instar, caste production in the colony is controlled by positive and negative feedback mechanisms: a greater density of other castes induces soldier production, whereas increasing soldier density suppresses further soldier production (Shibao et al. 2003, 2004a, b, c). In this species, the soldiers not only defend the colony against predators but also clean the gall by removing waste products. When the soldiers are still young, they undertake relatively safe tasks inside the colony such as gall cleaning. As the soldiers age, their tasks involve more dangerous activities outside the colony such as colony defense. Thus, a colony can maintain a sufficient work force and defense capability by constraining early deaths to the sterile caste. The division of labor in the aphid social system is adaptive and based on soldier-age polyethism (Shibao et al. 2004d). Molecular and cellular/histological mechanisms that generate different morphs during caste polyphenism in social insects have recently been elucidated by Miura and colleagues. Soldier-specific gene expression (Miura et al. 1999; Koshikawa et al. 2005), modification of the mandibular motor neurons (Ishikawa et al. 2008), and juvenile hormone (JH)-promoting caste differentiation (Cornette et al. 2008) have been successively discovered in the termite Hodotermopsis sjostedti. Compound eye development during caste differentiation in the termite, Reticulitermes speratus, has been demonstrated (Maekawa et al. 2008). 123 8 The gene network analysis has rapidly been developed in the 2000s. Abouheif and Wray (2002) characterized the expression of several genes within the network of wing polyphenism in reproductive (winged) and sterile (wingless) ant castes. They showed that the expression of genes (e.g., en, Ubx, ap, exd, etc.) within the network was conserved in the winged castes of four ant species (genera Neoformica, Myrmica, Crematogaster, and Pheidole), whereas points of interruption within the network in the wingless castes were evolutionarily unstable. Furthermore, based on such gene network analysis, the study of sociogenomics in social insects, especially the honey bee, Apis melifera, has undergone a rapid increase (Robinson et al. 2005; Whitfield et al. 2006; Grozinger et al. 2007). Robinson et al. (2005) and Weinstock et al. (2006) claimed a new approach that is based on transcriptomics: measuring changes in the expression of genes that correlate with changes in behavior. Gene expression is measured in the brains of individuals that have different behaviors of interest. Transcript abundance, however, is not always predictive of protein abundance. Some differences in gene expression may be a consequence, not a cause, of a behavioral change. Therefore, it is important to go beyond gene expression–behavior correlations to manipulate transcript abundance or protein activity through transgenesis, RNAi, pharmacology with neurotransmitters, and so on (Robinson et al. 2005; Weinstock et al. 2006). In addition, Elango et al. (2009) reported epigenetics that DNA methylation was widespread and associated with differential gene expression in social castes in A. merifela. The transcriptomics-based approach will be a powerful approach towards the gene discovery, especially for model social species. Inducible defense traits for predator avoidance Woltereck (1909) presented firstly the term ‘‘reaction norm’’ in the study of Daphnia inducible defense (see Pigliucci 2001). Over the last 20 years, there have been more than 100 reports of inducible defense traits for predator avoidance in Daphnia species, including the development of head and tail spines in D. rosea (Dodson 1972, 1984), D. pulex (Hammill et al. 2008), and D. lumholtzi (Engel and Tollrian 2009). Colony formation in a phytoplankton genus Scenedesmus has also been reported to be an inducible defense against grazers (Lurling and Van Donk 2000; Van der Stap et al. 2008). Tadpoles of Rana produce head bloating as an inducible defense in R. sylvatica (Van Buskirk and Relyea 1998), R. lessonae (Wilson et al. 2005), and R. pirica (Kishida and Nishimura 2006; Kishida et al. 2006, 2009, 2010). In addition, inducible offense by predators has also been reported; large jaws that enable tadpoles to be swallowed occur among morphs of the salamander, Hynobius retardatus (Kishida et al. 2010). 123 Popul Ecol (2010) 52:5–14 Embryological formation of inducible defense trait, neckteeth, was discovered by Laforsch and Tollrian (2004), and molecular and cellular mechanisms of inducible defense in Daphnia have recently been partially elucidated by Imai et al. (2009). Colbourne et al. (2005) presented the Daphnia genome database, and Eads et al. (2008) proposed ecological genomics in Daphnia as the first results focusing on adaptation in the stress response and environmental sex determination, even though no paper has yet reported on inducible defense traits. For molecular genetics of tadpoles, Kurata et al. (2005) and Mori et al. (2005) conducted cDNA subtraction and microarray analysis to detect genes expressed in inducible defense in Rana tadpoles. Mori et al. (2005) focused on the bulgy body skin tissue (the major induced morphological change and the most downstream end of the gene interaction system for phenotypic expression) and reported several candidate genes. The bulgy-shaped body seems to be highly related to the bullous pemphigoid antigen, which causes the skin-blistering disorder, and tetranectin and uromodulin may be related to the extracellular matrix through myogenesis, protein secretion, and ion transport. As the reverse transcriptase-like protein gene is known to disrupt mammalian transcriptomes, retrotransposons may be involved (Mori et al. 2005). Transgenerational effects and genetic accommodation in phenotypic plasticity Inducible defense in infected plants Agrawal et al. (1999) reported transgenerational effects in inducible defense in the cruciferous plant, Raphanus sativus. They collected mature seeds from a parent plant that had been affected by lepidopteran caterpillars during development. The seeds were sown in the field, and equal numbers of caterpillars were attached to each resulting plant. It was found that the larval body mass was smaller for plants that had been infected with larvae in the previous generation than in plants that had not previously been infected. The inducible defense was chemical in nature, and production of the chemical substance in the seeds was switched on during ripening. Transgenerational density effects in locusts The desert locust, Schistocerca gregaria, undergoes polyphenism in response to low (solitary) and crowded (gregarious) population density phases. The former is characterized by green body coloration, smaller hatchlings, and solitary and sedentary habits, while the latter is characterized by dark-colored bodies, larger hatchlings, and Popul Ecol (2010) 52:5–14 gregarious and migratory habits (Uvarov 1966). Variation in these traits is continuous and not discrete, and transgenerational steps proceed toward the gregarious phase for several generations (Tanaka and Maeno 2008). A strong correlation is evident between coloration and body size; green and small hatchlings come from eggs produced by solitary females, whereas black and larger hatchlings come from eggs produced by gregarious females (Faure 1932; Tanaka and Maeno 2008; Maeno and Tanaka 2009). Tawfik et al. (1999) investigated the molecular basis of gregarious body pigmentation, and reported the isolation of a neurohormone (comprising 11 amino acids) from the corpora cardiaca. This neurohormone was identical to [His(7)] corazonin, and its primary structure is similar to the vertebrate melanophore-stimulating hormone. Treatment with [His(7)] corazonin induced gregarious black patterns even in isolated (solitary) nymphs (Tawfik et al. 1999). Tanaka and Maeno (2006) manually tried to remove the maternal effect by washing eggs with saline or by separating eggs individually within 1 h of egg deposition. Neither washing nor separation of eggs at deposition affected the percentage of green hatchlings. The variation in hatchling body color was correlated closely to the body weight at hatchling. Then Maeno and Tanaka (2009) conducted two methods of artificial miniaturization of eggs: (1) removal of water from the eggs and (2) squeezing yolk from the eggs. Using these methods, they successfully reproduced a positive correlation between body size and body color. These experiments have largely elucidated polyphenism processes in the locust, and demonstrated phenotypic plasticity without genetic differentiation, i.e., from solitary to gregarious phases for several generations in transgenerational processes with maternal effects (Maeno and Tanaka 2009). Furthermore, Anstey et al. (2009) has recently reported that a neurotransmitter, serotonin, was responsible for the behavioral transformation from solitary to gregarious phases in the locust, S. gregaria. Solitary locusts acquire full gregarious behavioral characteristics within the first 2 h of forced crowding. This period coincides with a substantial but transient (\24 h) increase in the amount of serotonin, specifically in the central nervous system, the thoracic ganglia, but not the brain. They demonstrated a neurochemical mechanism linking interactions between individuals to large-scale changes in population structure and the onset of mass migration. Evolutionary changes through phenotypic plasticity: Baldwin effect, genetic assimilation, and genetic accommodation For evolutionary change through phenotypic plasticity, Price et al. (2003) pointed out that entry into a new 9 environment results in selection pressures favoring divergence from the ancestor, and that different environments also directly induce changes in an individual’s behavior, morphology, and physiology. Such changes are generically named ‘‘phenotypic plasticity’’. This plasticity is adaptive, in that individuals which show a plastic response have higher fitness than those which do not (Price et al. 2003), and it may have evolved as a consequence of variable conditions (Levins 1968; Via and Lande 1985; Robinson and Gukas 1999). How does plasticity interact with environmental conditions to produce genetic change? First, we need to clarify the terms ‘‘Baldwin effect’’ and ‘‘accommodation’’. Price et al. (2003) summarized the process of genetic assimilation which was first outlined by Spalding (1873), who argued that selection of those individuals which were the best learners would eventually result in the appearance of the behavior in the absence of learning. The idea that plastic traits in phenotype could become genetically fixed was raised by Baldwin (1896) and Morgan (1896) (the ‘‘Baldwin effect’’ termed by Simpson 1953; see Crispo 2007). Simpson (1953) defined the Baldwin effect as the situation where ‘‘characters individually acquired by members of the group may eventually, under the influence of selection, be reinforced or replace similar hereditary characters.’’ Baldwin (1896, 1902) often used the term ‘‘accommodation’’ in reference to non-heritable phenotypic changes that increase the survival of the organism in the particular environment in which the phenotypic change is induced. West-Eberhard (2003, 2005) divided accommodation into genetic and phenotypic components, and ‘‘phenotypic accommodation’’ (West-Eberhard 2003, 2005) is the modern-day equivalent of Baldwin’s accommodation (see Crispo 2007). Baldwin (1902) noted that heritable variation can occur in the same direction as the phenotypic response (he termed ‘‘conincident variations’’) and phenotypes that are originally environmentally induced can be selected upon and inherited. Currently, this phenomenon is considered a type of ‘‘genetic accommodation’’ (Crispo 2007), and an empirical experiment (Suzuki and Nijhort 2006) will be demonstrated (see later). On the other hand, Waddington (1953, 1959, 1961) proposed that development would evolve to become ‘‘canalized’’ against environmental perturbations, via selection acting on the developmental system, a process he referred to as ‘‘genetic assimilation’’ (Waddington 1953, 1961). Specifically, he defined genetic assimilation as a process ‘‘by which a phenotypic character, which initially is produced only in response to some environmental influence, becomes, through a process of selection, taken over by the genotype, …’’ (Waddington 1961). Although Waddington’s canalization and genetic assimilation may be 123 10 apparently similar to the Baldwin effect, the two concepts have fundamental differences (Crispo 2007). Waddington’s theory is based on the viewpoint that the environment induces phenotypes that are adaptive, and then selection on the developmental system acts to reduce responsiveness to the environment (i.e., to reduce plasticity). Therefore, we need to understand that Waddington’s genetic assimilation and canalization is a special case of the general concept of the Baldwin effect and genetic accommodation. The experiment of genetic accommodation Related species are likely to share genetic and developmental backgrounds. Therefore, Suzuki and Nijhort (2006) reasoned that exposing hidden genetic variation by stress (heat shock) could evolve a polyphenic regulatory mechanism in a monophenic species that shared a recent common ancestor with a polyphenic species. They investigated this possibility using artificial selection to evolve a larval color polyphenism in the tobacco hornworm, Manduca sexta, which is a monophenic species with green larvae. A related species, M. quinquemaculata, exhibits a larval color polyphenism, developing a black phenotype at 20C and a green phenotype at 28C. Wildtype larval coloration was robust to thermal stress, with fifth instar larvae remaining green following heat shock treatment during the mid and late fourth larval instar stage. Thus, their experiments examined the effect of thermal stress in both the polyphenic line and the black mutant line of M. sexta. The black mutation is a sexlinked recessive allele that reduces JH secretion, and the black mutant phenotype can revert to a normal greencolored larva by treatment with JH. Suzuki and Nijhort (2006) conducted an artificialselection experiment on the reaction norm (Schmalhausen 1949; Sarkar 2004), and the polyphenic line become more and more green under the high-temperature condition. The reaction norm in the temperature-dependent color score (the greener the larva, the higher the score) dramatically increased from 25 to 33C in the polyphenic line, although larvae of the black mutant were constantly black at physiologically tolerable temperatures ranging from 25 to 33C. Based on these experiments, a mechanistic view of the evolution of polyphenism by genetic accommodation in the threshold trait, JH titer, was developed (the term ‘genetic assimilation’ is used for the monophenic form, based on stabilization). Furthermore, as the empirical test, Suzuki and Nijhort (2008) conducted cross experiments between polyphenic and monophenic strains, including F1 crosses, and showed that the mechanism of genetic accommodation relies on changes that are consistent with the current view of the genetic basis of adaptive evolution. 123 Popul Ecol (2010) 52:5–14 Learning in behavioral adaptation as phenotypic plasticity Learning behaviors in vertebrates and insects The new field of behavioral neurobiology, which has emerged in recent decades (e.g., Carew 2000; Zupanc 2003), has focused on model organisms including the mouse (Mus musculus; spatial orientation learning and memory), the zebra finch (Taeniopygia guttat; song learning), the zebra fish (Danio rerio; developmental biology), the sea hare (Aplysia kurodai; sensitization and memory storage), the fruit fly (Drosophila melanogaster; associative learning) and the nematode (Caenorhabditis elegance; perception of density gradient movement in chemostasis). Numerous behavioral neurobiology studies involving D. melanogaster are reported annually, including a number concerning associative learning in relation to olfactory cues (e.g., Raine 2009; Yarali et al. 2009). Kawecki and colleagues (Mery and Kawecki 2003, 2004a; Kawecki 2010) have been unique in investigating the fitness cost of learning in D. melanogaster, especially the trade-off between learning performance and certain fitness components including fecundity and longevity (Flatt and Kawecki 2007; Burger et al. 2008). One of the most astonishing discoveries is that longterm memory is costly in D. melanogaster because it requires protein synthesis inside the mushroom body, but anesthesia-resistant memory (maintained for several hours) has no cost (Mery and Kawecki 2005) because it does not involve protein synthesis. The cost of long-term memory increases when combined with stressful conditions, such as desiccation. Another notable finding has been the detection of the Baldwin effect in D. melanogaster (Mery and Kawecki 2004b; Paenke et al. 2007; Kawecki 2010). Mery and Kawecki (2004b) established experiments involving two nutrient media (pineapple and orange) and two selection regimes (‘innate’ and ‘learning’), and applied this 2 9 2 artificial selection regime design to D. melanogaster populations. The experimental chamber had two small dishes containing either pineapple or orange medium. For the ‘learning pineapple’ treatment, the researchers added quinine to the alternative orange medium, so that the flies would only lay eggs in the pineapple medium (i.e., reinforced learning for ‘pineapple’). Comparison of the ‘learning’ and ‘innate’ regimes showed that the ‘learning pineapple’ regime was associated with a more rapid evolutionary pace (Mery and Kawecki 2004b), indicating that learning drives evolutionary processes at a greater rate. For genetic accommodation in wild animas in nature, entry into very different environments must be Popul Ecol (2010) 52:5–14 Fig. 1 Diagrammatic representation of the evolution of behavior and the Baldwin effect accompanied by behavioral and other plastic forms of accommodation, and this will usually be followed by selection in the context of these changes. Price et al. (2003) presented an example: the development of tool using in the woodpecker finch, Camarhynchus pallidus, on the Galapagos. Although tool using may have arisen and spread as a result of cultural innovation, the habit now develops independently of any tutoring (Tebbich et al. 2001), suggesting genetic accommodation. Figure 1 shows a diagram of a modernized version of the evolution of behaviors and the Baldwin effect. An organism receives information from its environment (cognition), and its behavioral response has resultant consequences (Success or failure? How much reward?). As a consequence of the response, neurotransmitters (e.g., dopamine, octopamine, or serotonin) are secreted in the brain–nervous system of the individual, which promotes memory storage, especially long-term memory. Memory storage affects the next behavioral action, which is a phenotypic character that is genetically affected by the individual genotype with variation at the population level. Therefore, behavioral characters are under natural selection. Furthermore, selection of genotypes in the adaptive landscape that enhancing phenotypic plasticity is accelerated with convex fitness function (Paenke et al. 2007); then, the behavioral consequence of learning provides feedback to natural selection on genetic variance. Choice behavior, learning-mediated population dynamics, and adaptive dynamics Ishii and Shimada (2010) showed antiphase oscillations of two prey species of bruchid seed beetle, Callosobruchus spp., parasitized by a pteromalid wasp, Anisopteromalus 11 calandrae, in a one predator–two prey experimental system. The oscillations can be generated by predation switching by the wasp, which was based on the wasp learning to attack the more abundant prey species. Continuous conditioning (about 24–48 h) during predation on the same host resulted in A. calandrae establishing a chemical search image of the common prey (Ishii and Shimada 2010). Although theoretical predictions have been investigated (Murdoch and Oaten 1975; Oaten and Murdoch 1975), an empirical test has never been reported. The empirical analysis of Ishii and Shimada (2010) is the first report of antiphase oscillations and persistence of the three-species system over a long period. P.A. Abrams has developed models for various types of adaptive changes including switching behavior for prey types amongst generalist consumers (Abrams 1999, 2006, 2010), movement behavior from one patch to another (Abrams 2007), and developmental plasticity (Abrams and Rowe 1996). Abrams et al. (1993) compared adaptive dynamics including learning (hereafter, small notation ‘‘adaptive dynamics’’) with traditional evolutionary dynamics without adaptive change (hereafter, capital notation ‘‘Adaptive Dynamics’’ incorporating only mutation– selection evolutionary process); the adaptive dynamic consequences, including behavioral adaptation, could change drastically in the model. Therefore, Abrams (2005) emphasized the importance of including adaptive change and comparing ‘adaptive dynamics’ with ‘Adaptive Dynamics’; the latter refers to a specific set of methods for analyzing mutation-limited evolutionary change. Concluding remarks This review has emphasized that rapid adaptation is ubiquitous in nature and has over-viewed recent research developments, including cellular–historical analyses and molecular biology techniques, in the areas of phenotypic plasticity and learning behavior. As Abrams (2005) has pointed out, behavioral and evolutionary ecological research on rapid adaptation (‘adaptive dynamics’; sensu Abrams 2005) will inform new understanding in the biological sciences. Unification of biological sciences will be enhanced; for example, behavioral ecology and behavioral neurobiology in the area of learning, and evolutionary ecology and molecular developmental biology in the area of phenotypic plasticity. Acknowledgments The authors are grateful to the Chief-in-Editor, Dr. T. Saitoh of Hokkaido University, and the editorial office, Ms M. Tanigawa, for supporting this symposium in the present issue, especially our long review. Special thanks should be given to Dr. T. 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