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Laboratory natural selection and artificial selection are vital tools for addressing specific questions about evolutionary patterns of variation. Laboratory natural selection can illuminate whether a putative selective agent is capable of generating long-term, sustained changes in individual traits and suites of traits. Artificial selection is the essential tool for understanding the general evolvability of traits and the extent to which genetic correlations constrain evolution. We review the contexts in which each type of experiment seems capable of offering key insights into important evolutionary issues. We also discuss theoretical and methodological considerations that play critical roles in designing selection experiments that are relevant to evolutionary patterns of trait variation. In particular, we focus on the critical role of selection intensity and the consequences of experiments with different intensities. While selection experiments are not practical in many cases, sophisticated selection experiments—designed with careful consideration of the theory of selection—should be taken beyond model organisms and used in well-chosen natural systems to understand natural patterns of variation.
Based upon ideas about evolution, we put forth the argument that the capacity to transfer energy via aerobic metabolism is such a central feature of mammalian biology, that it must also be the primary determinant of complex disease. From this, we hypothesized that artificial selection on low and high capacity for aerobic exercise would create lines that can be used to define the divide between health and disease. In 1996 we began large-scale divergent selection for aerobic treadmill running capacity in a widely heterogeneous stock of rats (N:NIH). By ten generations we developed lines of low capacity runners (LCR) and high capacity runners (HCR) that on average differed by 317%. As a correlated trait, body mass increased at each generation in the LCR while the body mass decreased in the HCR. The lines also separated for key factors of systemic oxygen transport capacity such as maximal oxygen consumption (VO2max), tissue perfusion, capillary density, and oxidative enzyme activity (citrate synthase and B-HAD). We also tested our hypothesis that differences in aerobic energy transfer would produce rats that contrast for risk factors associated with complex disease. Indeed, the lines separated for cardiovascular risk factors including differences in blood pressure, cardiac contractility, visceral adiposity, plasma free fatty acids, and triglycerides. The decrease in aerobic capacity was also associated with low amounts of several proteins required for mitochondrial function.
Artificial selection experiments are potentially powerful, yet under-utilized tool of evolutionary and physiological ecology. Here we analyze and review three important aspects of such experiments. First, we consider the effects of instrumental measurement errors and random fluctuations of body mass on the total phenotypic variation. We illustrate this with the analysis of measurements of oxygen consumption in an open-flow respirometry set-ups. We conclude that measurement errors and fluctuations of body mass are likely to reduce the repeatability of oxygen consumption by about one third. Using published estimates of repeatability of metabolic rates we also showed that it does not tend to decline with increasing time between measurements. Second, we review data on narrow sense heritability (h2) of metabolic rates in mammals. The results are equivocal: many studies report very low (∼0.1) h2, whereas some recent studies (including our own estimates of h2 in laboratory mice, obtained by means of parent-offspring regression) report significant h2 ≥ 0.4. Finally, we discuss consequences of the lack of replicated lines in artificial selection experiments. We focus on the confounding effect of genetic drift on statistical inferences related to primary (selected) and secondary (correlated) traits, in the absence of replications. We review literature data and analyze them following the guidelines formulated by Henderson (1989, 1997). We conclude that most results obtained in unreplicated experiments are probably robust enough to ascribe them to the effect of selection, rather than genetic drift. However, Henderson's guidelines by no means should be treated as a legitimate substitute of the analysis of variance, based on replicated lines.
We used a novel mouse model to study the effects of selective breeding for high locomotor activity (14 generations) on relative organ sizes, hematocrit (Hct), and blood hemoglobin (Hb) concentration. We also examined effects of exercise training and genotype-by-environment interactions by housing animals for 8 weeks with wheels that were either free to rotate or locked. Mice from the four replicate High-Runner (HR) lines were smaller in total body mass but had larger body mass-adjusted kidneys relative to the four Control lines (P < 0.05). Control and HR lines did not differ significantly for mass-adjusted tail length or masses of the “triceps surae” hindlimb muscle group, heart (ventricle), spleen, liver, adrenal glands or gonads. Wheel access caused a reduction in body mass and an increase in relative heart mass. In females only, wheel access caused a reduction in relative spleen mass. Wheel access did not affect relative tail length or relative mass of the triceps surae, liver, adrenal gland or gonads. Significant interactions between selection history and wheel access were observed in females for spleen, liver, and gonad mass as well as Hct and Hb. Wheel access caused increases in both Hct and Hb, mainly in the HR lines. The mini-muscle phenotype, caused by a Mendelian recessive allele that halves hindlimb muscle mass, was significantly associated with several other body composition traits, including reduced body mass, increased tail length, increased heart mass, increased liver mass (females only), increased mean adrenal gland mass (females only), increased mean kidney mass (males only), and reduced Hct (wheel-access females only). Results are discussed in context of the beneficial acclimation hypothesis, genotype-by-environment interactions, and the potential for “nurture” to be self-reinforcing of “nature” in some complex behavioral-physiological phenotypes.
Selective breeding of house mice has been used to study the evolution of locomotor behavior. Our model consists of 4 replicate lines selectively bred for high voluntary wheel running (High-Runner) and 4 bred randomly (Control). The major changes in High-Runner lines appear to have taken place in the brain rather than in capacities for exercise. Their neurobiological profile resembles features of human Attention Deficit Hyperactivity Disorder (ADHD) and is also consistent with high motivation for exercise as a natural reward. Both ADHD and motivation for natural rewards (such as food and sex), as well as drugs of abuse, have been associated with alterations in function of the neuromodulator dopamine, and High-Runner mice respond differently to dopamine drugs. In particular, drugs that block the dopamine transporter protein (such as Ritalin and cocaine) reduce the high-intensity running of High-Runner mice but have little effect on Control mice. In preliminary studies of mice exercised on a treadmill, brain dopamine concentrations did not differ, suggesting that changes in the dopamine system may have occurred downstream of dopamine production (e.g., receptor expression or transduction). Brain imaging by immunohistochemical detection of c-Fos identified several key regions (prefrontal cortex, nucleus accumbens, caudate-putamen, lateral hypothalamus) that appear to play a role in the differential response to Ritalin and in the increased motivation for running in High-Runner mice. The activation of other brain regions, such as the hippocampus, was closely associated with wheel running itself. Chronic wheel running (several weeks) also increased the production of new neurons to apparently maximal levels in the hippocampus, but impaired learning in High-Runner mice. We discuss the biomedical implications of these findings.
Numerous studies have documented evolution by natural selection in natural populations, but few are genuine selection experiments that are designed and then executed in nature. We will focus on these few cases to illustrate what can be learned from field selection experiments alone or field and laboratory selection experiments together that cannot be learned from laboratory experiments alone. Both types of study allow us to evaluate cause and effect relationships because a planned experiment can be accompanied by a more direct evaluation of the factors that cause evolution. A unique benefit of field experiments is that they give us the opportunity to measure the rate and magnitude of selection in nature. We have found that this rate is far greater than one might imagine based on observations of the fossil record. A combination of field and laboratory selection experiments has revealed the importance of population size and structure in shaping the genetics of adaptation. For example, laboratory selection experiments on insecticide resistance tend to attain resistance though polygenic inheritance. The evolution of insecticide resistance in nature often eventually yields to single genes of large effect that are rare but, once they arise, represent a higher fitness solution to resistance and spread among populations. Finally, field studies enable us to test evolutionary theory in a context in which all of the tradeoffs associated with a trait are realized; in the laboratory, organisms may be shielded from the fitness tradeoffs associated with the evolution of a trait. For example, we have compared the patterns of senescence in guppies from high and low mortality rate environments in the laboratory and in the field. In the laboratory, guppies from high predation environments had delayed senescence relative to those from low predation environments. In the field the apparent relationship is the opposite. One hypothesis for this difference is that a tradeoff associated with the evolution of the high predation life history is a decrease in the investment in the immune system. Such a sacrifice would be evident in nature where there is exposure to disease and parasites but less so in the laboratory, which is relatively disease and parasite free.
In rainbow trout the magnitude of the cortisol response to stress shows both consistency over time and a moderate to high degree of heritability, and high responding (HR) and low responding (LR) lines of rainbow trout have been generated by individual selection for consistently high or low post-stress cortisol values. Using 2nd and 3rd generation fish, we tested the hypothesis that differential stress responsiveness is associated with behavioral alterations in the HR-LR trout model. LR fish showed a tendency to become socially dominant, a rapid recovery of food intake after transfer to a novel environment, and a reduced locomotor response in a territorial intrusion test. Furthermore, stress induced elevation of brain stem and optic tectum concentrations of the monoamine neurotransmitters serotonin, dopamine, and norepinephrine and their metabolites suggests that both synthesis and metabolism of these transmitters were elevated after stress to a larger degree in HR than in LR trout. A divergent pattern was seen in the hypothalamus, where LR fish displayed elevated levels of 5-hydroxyindoleacetic acid (a serotonin metabolite) and 3-methoxy-4-hydroxyphenylglycol (a norepinephrine metabolite). Thus, selection for a single trait, cortisol responsiveness, in rainbow trout is associated with concurrent changes in both behavior and central signaling systems. The apparent parallel to genetically determined stress coping styles in mammals, and the existence of similar trait associations in unselected populations of rainbow trout, suggests an evolutionarily conserved correlation between multiple traits. Continuing studies on the HR and LR trout lines are aimed at providing the physiological and genetic basis for new marker-assisted selection strategies in the rapidly developing finfish aquaculture industry, as well as increased knowledge of the function and evolution of central neuroendocrine signaling systems.
The plasticity of any given trait, which has a genetic basis and which may or may not be adaptive, can intensify or attenuate evolved responses, and can itself evolve in response to selection depending on the scale of spatial or temporal heterogeneity. To investigate the complex function and evolution of plastic traits, an appealing yet challenging approach is assessing responses to artificial selection. Here, I review how artificial selection has been employed to explore four botanical research themes: (1) relationships between plastic and evolved responses to multiple stresses, (2) integration of cellular, leaf-level, and whole-plant responses to altered CO2 concentrations, (3) photomorphogenic and photoperiodic development, both mediated by phytochrome photoreceptors, and (4) the evolution of the pest-induced myrosinase-glucosinolate system in cruciferous plants. These diverse topics are unified not only because they have been studied using artificial selection experiments, but also because they have considered variability in multiple traits affected by multiple factors in the external environment. Limitations of such research include a dearth of long-term studies; a surprising but often logistically necessary omission of control or replicate lines; and numerous issues relating to assessing impacts of inbreeding and drift. In addition to discussing options for circumventing such limitations, I draw attention to strategies for integrating the results of artificial selection studies with progress in functional and evolutionary genomics.
One of the enduring temptations of evolutionary theory is the extrapolation from short-term to long-term, from a few species to all species. Unfortunately, the study of experimental evolution reveals that extrapolation from local to general patterns of evolution is not usually successful. The present article supports this conclusion using evidence from the experimental evolution of life-history in Drosophila. The following factors demonstrably undermine evolutionary correlations between functional characters: inbreeding, genotype-by-environment interaction, novel foci of selection, long-term selection, and alternative genetic backgrounds. The virtual certainty that at least one of these factors will arise during evolution shreds the prospects for global theories of the effects of adaptation. The effects of evolution apparently don't generalize, even though evolution is a global process.
Laboratory selection for desiccation resistance, which has been imposed on five replicate populations of Drosophila melanogaster for >200 generations, has resulted in enhanced survivability during periods of extreme water stress. The ability of these populations to persistently resist the fatal effects of desiccation is correlated with evolved physiological traits, namely preferential storage of carbohydrates (associated with reduced lipid reserves) and a dramatic increase in blood volume, which has led to a significant increase in extracellular sodium and chloride content, as well as body mass. When compared to other populations of this drosophilid species, these adaptive traits are unique. While some may argue against the value of evolved traits that have not been found in natural populations, we counter that such traits are of considerable value to the analyses of physiological functions, as well as the underlying mechanisms and evolutionary trajectories of these functions. We propose that multiple physiological consequences almost certainly derive from the evolution of these singular traits; and, furthermore, we discuss future directions for the elucidation of such consequences.
Coevolution between male and female traits can result from correlated responses to selection or correlated selection on genetically independent traits. This study examines the possibility that traits involved in precopulatory sexual selection may influence the evolution of traits involved in postcopulatory sexual selection due to the existence of correlated selection or correlated responses to selection. Artificial selection on male eye span in Cyrtodiopsis dalmanni, a sexually dimorphic stalk-eyed fly, is used to test for correlated changes in reproductive traits of male and female flies. Flies from replicate lines that had been under selection for 57 generations were matched for age and genotyped at four X-linked microsatellite loci. Egg number and testis size increased with age, but did not differ among lines. Spermathecal areas and duct lengths differed among replicates, but not among selection treatments. Female relative eye span, size of the ventral receptacle and egg size exhibited significant correlated responses to selection on male relative eye span. The absence of any change in sperm length or testis size between lines indicates that changes in female traits are unlikely due to correlated selection mediated by sperm competition. Significant effects of X-linked microsatellite genotypes indicate instead that the correlated responses to selection were due, in part, to X-linked genes in linkage disequilibrium or that exhibit pleiotropy. The presence of nonadditive allelic effects on genetically correlated female traits combined with additive allelic effects on a male ornament provides a previously unrecognized mechanism by which genetic variation could be maintained despite strong sexual selection.
The extent to which modifications in intermediary metabolism contribute to life history variation and trade-offs is an important but poorly understood aspect of life history evolution. Artificial selection was used to produce replicate genetic stocks of the wing-polymorphic cricket, Gryllus firmus, that were nearly pure-breeding for either the flight-capable (LW[f]) morph, which delays ovarian growth, or the flightless (SW) morph, which exhibits enhanced early-age fecundity. LW(f) lines accumulated substantially more triglyceride, the main flight fuel in Gryllus, compared with SW-selected lines, and enhanced accumulation of triglyceride was strongly associated with reduced ovarian growth. Increased triglyceride accumulation in LW(f) lines resulted from elevated de novo biosynthesis of fatty acid and two morph-specific trade-offs: (1) greater proportional utilization of fatty acid for glyceride biosynthesis vs. oxidation, and (2) a greater diversion of fatty acids into triglyceride vs. phospholipid biosynthesis. Even though SW lines produced less total lipid and triglyceride, they produced more phospholipid (important in egg development) than did LW(f) lines. Differences between LW(f) and SW morphs in lipid biosynthesis resulted from substantial alterations in the activities of all studied lipogenic enzymes, a result that is consistent with expectations of Metabolic Control Theory. Finally, application of a juvenile hormone analogue to LW(f) females produced a striking SW phenocopy with respect to all aspects of lipid metabolism studied. Global alterations of lipid metabolism, most likely produced by alterations in endocrine regulation, underlie morph specializations for flight vs. early-age fecundity in G. firmus. Modification of the endocrine control of intermediary metabolism is likely to be an important mechanism by which intermediary metabolism evolves and contributes to life history evolution.
Natural selection typically acts on multiple traits simultaneously. Quantitative genetics provides the theory for predicting the response to selection of multiple traits and predicts symmetrical responses to selection (the response to upward selection on both traits is equal to their response to downward selection). In reality, however, the response to simultaneous selection on two traits is often asymmetrical. We provide a physiology-based framework to explain the asymmetrical response to simultaneous selection on two important life history traits: body size and development time. The tobacco hornworm, Manduca sexta, is particularly well suited for such a study, as the physiological control of body size and development time is well known in this species. Three physiological factors control both life history traits in M. sexta: growth rate, the critical weight that measures the timing of the onset of the cessation of juvenile hormone secretion (which initiates the processes leading to pupation) and the time interval between the critical weight and secretion of the molting hormone 20-hydroxyecdysteroid (the interval to cessation of growth, ICG). Asymmetry in the response to simultaneous selection on the two life history traits is due to the different types of selection acting on the three physiological factors. The critical weight and ICG are always under synergistic selection when both focal traits are selected in the same direction and under antagonistic selection when the focal traits are selected in opposite directions. Growth rate follows the opposite pattern. We propose a general model to explain the asymmetric response to simultaneous selection. This model emphasizes the importance of physiological processes in understanding evolutionary responses to selection and the control of complex traits.
Laboratory selection experiments play a prominent role in understanding organismal adaptation. Although bacteria are not yet commonly used for such experiments, they are well suited for analyses of both the organismic and the genetic basis of adaptation. Bacteria can be maintained in large populations while occupying limited laboratory space, have short generation times, are well characterized physiologically, biochemically, and genetically, and are readily frozen and revived from the freezer. In addition, the genomes of many species are completely sequenced and knowledge of gene function is unparalleled. Here we review general aspects of selection experiments, the history of using selection experiments in combination with thermal biology and genomics, and highlight findings from six lines of Escherichia coli adapted to high temperature (41.5°C), including changes in organismal fitness, physiological performance, gene complement and gene expression. Our results are an example of the powerful insights that can be discovered by combining the tools and analyses of many biological disciplines including genomics, evolutionary biology, genetics, and evolutionary physiology.
The Earth's magnetic field provides a pervasive source of directional information used by phylogenetically diverse marine animals. Behavioral experiments with sea turtles, spiny lobsters, and sea slugs have revealed that all have a magnetic compass sense, despite vast differences in the environment each inhabits and the spatial scale over which each moves. For two of these animals, the Earth's field also serves as a source of positional information. Hatchling loggerhead sea turtles from Florida responded to the magnetic fields found in three widely separated regions of the Atlantic Ocean by swimming in directions that would, in each case, facilitate movement along the migratory route. Thus, for young loggerheads, regional magnetic fields function as navigational markers and elicit changes in swimming direction at crucial geographic boundaries. Older turtles, as well as spiny lobsters, apparently acquire a “magnetic map” that enables them to use magnetic topography to determine their position relative to specific goals. Relatively little is known about the neural mechanisms that underlie magnetic orientation and navigation. A promising model system is the marine mollusc Tritonia diomedea, which possesses both a magnetic compass and a relatively simple nervous system. Six neurons in the brain of T. diomedea have been identified that respond to changes in magnetic fields. At least some of these appear to be ciliary motor neurons that generate or modulate the final behavioral output of the orientation circuitry. These findings represent an encouraging step toward a holistic understanding of the cells and circuitry that underlie magnetic orientation behavior in one model organism.
The ability to process in parallel multiple forms of sensory information, and link sensory-sensory associations to behavior, presumably allows for the opportunistic use of the most reliable and predictive sensory modalities in diverse behavioral contexts. Evolutionary considerations indicate that such processing may represent a fundamental operating principle underlying complex sensory associations and sensory-motor integration. Here, we suggest that animal navigation is a particularly useful model of such opportunistic use of sensory and motor information because it is possible to study directly the effects of memory on neural system functions. First, comparative evidence for parallel processing across multiple brain structures during navigation is provided from the literatures on fish and rodent navigation. Then, based on neurophysiological evidence of coordinated, multiregional processing, we provide a neurobiological explanation of learning and memory effects on neural circuitry mediating navigation.
The extraordinary navigational ability of homing pigeons provides a unique spatial cognitive system to investigate how the brain is able to represent past experiences as memory. In this paper, we first summarize a large body of lesion data in an attempt to characterize the role of the avian hippocampal formation (HF) in homing. What emerges from this analysis is the critical importance of HF for the learning of map-like, spatial representations of environmental stimuli used for navigation. We then explore some interesting properties of the homing pigeon HF, using for discussion the notion that the homing pigeon HF likely displays some anatomical or physiological specialization(s), compared to the laboratory rat, that account for its participation in homing and the representation of large-scale, environmental space. Discussed are the internal connectivity among HF subdivisions, the occurrence of neurogenesis, the presence of rhythmic theta activity and the electrophysiological profile of HF neurons. Comparing the characteristics of the homing pigeon HF with the hippocampus of the laboratory rat, two opposing perspectives can be supported. On the one hand, one could emphasize the subtle differences in the properties of the homing pigeon HF as possible departure points for exploring how the homing pigeon HF may be adapted for homing and the representation of large-scale space. Alternatively, one could emphasize the similarities with the rat hippocampus and suggest that, if homing pigeons represent space in a way different from rats, then the neural specializations that would account for the difference must lie outside HF. Only future research will determine which of these two perspectives offers a better approximation of the truth.
Behavior and electrophysiological studies have demonstrated a sensitivity to characteristics of the Geomagnetic field that can be used for navigation, both for direction finding (compass) and position finding (map). The avian magnetic compass receptor appears to be a light-dependent, wavelength-sensitive system that functions as a polarity compass (i.e., it distinguishes poleward from equatorward rather than north from south) and is relatively insensitive to changes in magnetic field intensity. The receptor is within the retina and is based on one or more photopigments, perhaps cryptochromes. A second receptor system appears to be based on magnetite and might serve to transduce location information independent of the compass system. This receptor is associated with the ophthalmic branch of the trigeminal nerve and is sensitive to very small (<50 nanotesla) changes in the intensity of the magnetic field. In neither case has a neuron that responded to changes in the magnetic field been traced to a structure that can be identified to be a receptor. Almost nothing is known about how magnetic information is processed within the brain or how it is combined with other sensory information and used for navigation. These remain areas of future research.
How homing pigeons displaced into unfamiliar territory find their way home has been the subject of extensive experimentation and debate. One reason for the controversy is that pigeons seem to use multiple cues. Clock-shifting experiments show that experienced pigeons use the sun as a preferred compass; when it is not available they rely on magnetic cues. That pigeons can home successfully while wearing frosted lenses suggests that landmarks, while not an essential navigational cue, are important in the final stages. The sensory basis of the “map” or position finding system is probably equally or even more complicated. When conditions around the loft are suitable, pigeons may use olfactory cues to find their way or might use some feature of the earth's magnetic field for their navigation. The Wiltschkos (1989) showed that pigeons raised without free access to ambient odors are not disoriented when anosmic while their siblings raised with free access to the prevailing wind were disoriented. Similarly, sibling pigeons from two lofts in Lincoln, Massachusetts. were well oriented or totally disoriented when released at magnetic anomalies under sunny skies depending upon which of the two lofts they had been reared in. All of these experiments and many more suggest that pigeons use multiple and redundant cues to find their way home. Further, there is the suggestion that which cues they adopt may well be influenced by the characteristics of the area around the home loft in which they were reared.