Genomics of local adaptation with gene flow

Gene flow is a fundamental evolutionary force in adaptation that is especially important to understand as humans are rapidly changing both the natural environment and natural levels of gene flow. Theory proposes a multifaceted role for gene flow in adaptation, but it focuses mainly on the disruptive effect that gene flow has on adaptation when selection is not strong enough to prevent the loss of locally adapted alleles. The role of gene flow in adaptation is now better understood due to the recent development of both genomic models of adaptive evolution and genomic techniques, which both point to the importance of genetic architecture in the origin and maintenance of adaptation with gene flow. In this review, we discuss three main topics on the genomics of adaptation with gene flow. First, we investigate selection on migration and gene flow. Second, we discuss the three potential sources of adaptive variation in relation to the role of gene flow in the origin of adaptation. Third, we explain how local adaptation is maintained despite gene flow: we provide a synthesis of recent genomic models of adaptation, discuss the genomic mechanisms and review empirical studies on the genomics of adaptation with gene flow. Despite predictions on the disruptive effect of gene flow in adaptation, an increasing number of studies show that gene flow can promote adaptation, that local adaptations can be maintained despite high gene flow, and that genetic architecture plays a fundamental role in the origin and maintenance of local adaptation with gene flow.     

Protective effects of intermittent hypoxic adaptation on myocardium and its mechanisms.

Intermittent hypoxic adaptation offers as many beneficial effects in protecting against myocardial injuries as chronic continuous hypoxic adaptation. However, chronic continuous hypoxic adaptation readily causes some adverse effects on the organism, which may be prevented by intermittent hypoxic adaptation. As an approach to potentiate the protective effects, intermittent hypoxic adaptation is also much easier to apply to subjects who are not living at high altitude. The mechanisms underlying the cardioprotective effects of intermittent hypoxic adaptation are less understood, although great similarities exist between chronic continuous and intermittent hypoxic adaptation. The participation of several factors, such as myocardial vascularity, coronary blood flow, and cardiomyoglobin, which comprise the oxygen uptake system is not apparent, while the more efficient energetic metabolism after intermittent hypoxic adaptation may be a mechanism for cardioprotection. The possible roles of several signaling transduction pathways, including adrenoceptors, prostaglandins, and the adenosinergic system, in the beneficial effects of intermittent hypoxia are compared to those of chronic continuous hypoxic adaptation. Antioxidant enzymes and stress proteins may also be part of the mechanisms contributing to the cardioprotection of the intermittent hypoxic adaptation. As the cardioprotective effects of intermittent hypoxic adaptation employ multifold mechanisms, their clear elucidation needs more efforts.     

Psychophysical and behavioral characteristics of olfactory adaptation

Sensory adaptation allows organisms to reach behavioral equilibrium with the ambient environment and respond primarily to changes in stimulation. Given its functional significance, it is not surprising that adaptation in the olfactory system exhibits many of the same characteristics as adaptation in other sensory systems, including vision. Repeated or prolonged exposure to an odorant typically leads to stimulus-specific decreases in olfactory sensitivity to that odorant, but sensitivity recovers over time in the absence of further exposure. Psychophysical analysis shows that olfactory adaptation results in elevations in odor thresholds and in reduced responsiveness to suprathreshold stimulation. Further, the magnitude of the decrease and the time course of adaptation and recovery are dependent on the concentration of the odor and on the duration of exposure. It is generally agreed that olfactory adaptation can occur at multiple levels in the olfactory system and can involve both peripheral (receptor level) and more central (post-receptor) components. Evidence for peripheral and central involvement comes from studies showing that monorhinal stimulation results in adaptation in both the ipsilateral and contralateral nostril, although the degree of adaptation in the ipsilateral nostril is more profound and recovery is slower. Additional evidence for central involvement comes from studies that have found relatively small decreases in peripheral response following repeated stimulation despite substantial reductions in perceived intensity. Most psychophysical studies of adaptation, however, have not differentiated the peripheral and central processes. Although relatively few in number, studies of the parametric features of olfactory adaptation in both vertebrate (e.g. rat) and invertebrate (e.g. Drosophila, Caenorhabditis elegans) animal models appear to replicate the findings in psychophysical studies of adult humans. Despite the broad overall similarity of olfactory adaptation to adaptation in other sensory systems, olfactory adaptation exhibits some unique features. Adaptation in olfaction has been shown to be very long-lasting in some cases and may be modulated by the contribution of pre-neural events and physico-chemical properties of the odorant molecules that govern diffusion to receptor sites and post-receptor clearance.     

Spatiotemporal variation in local adaptation of a specialist insect herbivore to its long‐lived host plant

Local adaptation of interacting species to one another indicates geographically variable reciprocal selection. This process of adaptation is central in the organization and maintenance of genetic variation across populations. Given that the strength of selection and responses to it often vary in time and space, the strength of local adaptation should in theory vary between generations and among populations. However, such spatiotemporal variation has rarely been explicitly demonstrated in nature and local adaptation is commonly considered to be relatively static. We report persistent local adaptation of the short‐lived herbivore Abrostola asclepiadis to its long‐lived host plant Vincetoxicum hirundinaria over three successive generations in two studied populations and considerable temporal variation in local adaptation in six populations supporting the geographic mosaic theory. The observed variation in local adaptation among populations was best explained by geographic distance and population isolation, suggesting that gene flow reduces local adaptation. Changes in herbivore population size did not conclusively explain temporal variation in local adaptation. Our results also imply that short‐term studies are likely to capture only a part of the existing variation in local adaptation.     

The effect of neural adaptation on population coding accuracy

Most neurons in the primary visual cortex initially respond vigorously when a preferred stimulus is presented, but adapt as stimulation continues. The functional consequences of adaptation are unclear. Typically a reduction of firing rate would reduce single neuron accuracy as less spikes are available for decoding, but it has been suggested that on the population level, adaptation increases coding accuracy. This question requires careful analysis as adaptation not only changes the firing rates of neurons, but also the neural variability and correlations between neurons, which affect coding accuracy as well. We calculate the coding accuracy using a computational model that implements two forms of adaptation: spike frequency adaptation and synaptic adaptation in the form of short-term synaptic plasticity. We find that the net effect of adaptation is subtle and heterogeneous. Depending on adaptation mechanism and test stimulus, adaptation can either increase or decrease coding accuracy. We discuss the neurophysiological and psychophysical implications of the findings and relate it to published experimental data.     

Physical work capacity of athletes with different types of adaptation of the cardiorespiratory system

Indices of physical work capacity in athletes with different types of adaptation of the cardiorespiratory system that are engaged in various kinds of sports and have sports ranks from Master of Sports to Grade 2 have been studied. It has been shown that the highest physical work capacity is typical of athletes that have the inotropic type of adaptation, and the lowest, of athletes with the chronotropic type of adaptation. High indices of physical work capacity were recorded in athletes with the respiratory type of adaptation. Types of adaptation affect the indices of physical work capacity, and it is possible to forecast sports results on their basis.     

Adaptation in the Ventral Eye of Limulus is Functionally Independent of the Photochemical Cycle, Membrane Potential, and Membrane Resistance

The early receptor potential (ERP), membrane potential, membrane resistance, and sensitivity were measured during light and/or dark adaptation in the ventral eye of Limulus. After a bright flash, the ERP amplitude recovered with a time constant of 100 ms, whereas the sensitivity recovered with an initial time constant of 20 s. When a strong adapting light was turned off, the recovery of membrane potential and of membrane resistance had time-courses similar to each other, and both recovered more rapidly than the sensitivity. The receptor depolarization was compared during dark adaptation after strong illumination and during light adaptation with weaker illumination; at equal sensitivities the cell was more depolarized during light adaptation than during dark adaptation. Finally, the waveforms of responses to flashes were compared during dark adaptation after strong illumination and during light adaptation with weaker illumination. At equal sensitivities (equal amplitude responses for identical flashes), the responses during light adaptation had faster time-courses than the responses during dark adaptation. Thus neither the photochemical cycle nor the membrane potential nor the membrane resistance is related to sensitivity changes during dark adaptation in the photoreceptors of the ventral eye. By elimination, these results imply that there are (unknown) intermediate process(es) responsible for adaptation interposed between the photochemical cycle and the electrical properties of the photoreceptor.     

Neural and Photochemical Mechanisms of Visual Adaptation in the Rat

The effects of light adaptation on the increment threshold, rhodopsin content, and dark adaptation have been studied in the rat eye over a wide range of intensities. The electroretinogram threshold was used as a measure of eye sensitivity. With adapting intensities greater than 1.5 log units above the absolute ERG threshold, the increment threshold rises linearly with increasing adapting intensity. With 5 minutes of light adaptation, the rhodopsin content of the eye is not measurably reduced until the adapting intensity is greater than 5 log units above the ERG threshold. Dark adaptation is rapid (i.e., completed in 5 to 10 minutes) until the eye is adapted to lights strong enough to bleach a measurable fraction of the rhodopsin. After brighter light adaptations, dark adaptation consists of two parts, an initial rapid phase followed by a slow component. The extent of slow adaptation depends on the fraction of rhodopsin bleached. If all the rhodopsin in the eye is bleached, the slow fall of threshold extends over 5 log units and takes 2 to 3 hours to complete. The fall of ERG threshold during the slow phase of adaptation occurs in parallel with the regeneration of rhodopsin. The slow component of dark adaptation is related to the bleaching and resynthesis of rhodopsin; the fast component of adaptation is considered to be neural adaptation.     

Limits to local adaptation in six populations of the annual plant Diodia teres

* Local adaptation is common, but tests for adaptive differentiation frequently compare populations from strongly divergent environments, making it unlikely that any influence of stochastic processes such as drift or mutation on local adaptation will be detected. Here, the hypothesis that local adaptation is more likely to develop when the native environments of populations are more distinct than when they are similar was tested. * A reciprocal transplant experiment including two populations from each of three habitats was conducted to determine the pattern of local adaptation. In addition to testing for local adaptation at the population level, the hypothesis was tested that local adaptation is more common between populations from different habitats than between populations from the same habitat. * Local adaptation was not common, but more evidence was found of local adaptation between populations from different habitats than between populations from the same habitat. Two instances of foreign genotype fitness advantage confirm that stochastic processes such as drift can limit local adaptation. * These results are consistent with the hypothesis that stochastic processes can inhibit local adaptation but are more likely to be overwhelmed by natural selection when populations occur in divergent environments.     

Influence of haptic guidance in learning a novel visuomotor task

In (re)learning of movements, haptic guidance can be used to direct the needed adaptations in motor control. Haptic guidance influences the main driving factors of motor adaptation, execution error, and control effort in different ways. Human-control effort is dissipated in the interactions that occur during haptic guidance. Minimizing the control effort would reduce the interaction forces and result in adaptation. However, guidance also decreases the magnitude of the execution errors, which could inhibit motor adaptation. The aim of this study was to assess how different types of haptic guidance affect kinematic adaptation in a novel visuomotor task. Five groups of subjects adapted to a reaching task in which the visual representation of the hand was rotated 30°. Each group was guided by a different force field. The force fields differed in magnitude and direction in order to discern the adaptation based on execution errors and control effort. The results demonstrated that the execution error did indeed play a key role in adaptation. The more the guiding forces restricted the occurrence of execution errors, the smaller the amount and rate of adaptation. However, the force field that enlarged the execution errors did not result in an increased rate of adaptation. The presence of a small amount of adaptation in the groups who did not experience execution errors during training suggested that adaptation could be driven on a much slower rate and on the basis of minimization of control effort as was evidenced by a gradual decrease of the interaction forces during training. Remarkably, also in the group in which the subjects were passive and completely guided, a small but significant adaptation occurred. The conclusion is that both minimization of execution errors and control effort drives kinematic adaptation in a novel visuomotor task, but the latter at a much slower rate.     

Molecular Parallelism Underlies Convergent Highland Adaptation of Maize Landraces

Convergent phenotypic evolution provides some of the strongest evidence for adaptation. However, the extent to which recurrent phenotypic adaptation has arisen via parallelism at the molecular level remains unresolved, as does the evolutionary origin of alleles underlying such adaptation. Here, we investigate genetic mechanisms of convergent highland adaptation in maize landrace populations and evaluate the genetic sources of recurrently selected alleles. Population branch excess statistics reveal substantial evidence of parallel adaptation at the level of individual single-nucleotide polymorphism (SNPs), genes, and pathways in four independent highland maize populations. The majority of convergently selected SNPs originated via migration from a single population, most likely in the Mesoamerican highlands, while standing variation introduced by ancient gene flow was also a contributor. Polygenic adaptation analyses of quantitative traits reveal that alleles affecting flowering time are significantly associated with elevation, indicating the flowering time pathway was targeted by highland adaptation. In addition, repeatedly selected genes were significantly enriched in the flowering time pathway, indicating their significance in adapting to highland conditions. Overall, our study system represents a promising model to study convergent evolution in plants with potential applications to crop adaptation across environmental gradients.     

The effects of migration and drift on local adaptation to a heterogeneous environment

Local adaptation experiments are widely used to quantify the levels of adaptation within a heterogeneous environment. However, theoretical studies generally focus on the probability of fixation of alleles or the mean fitness of populations, rather than local adaptation as it is commonly measured experimentally or in field studies. Here, we develop mathematical models and use them to generate analytical predictions for the level of local adaptation as a function of selection, migration and genetic drift. First, we contrast mean fitness and local adaptation measures and show that the latter can be expressed in a simple and general way as a function of the spatial covariance between population mean phenotype and local environmental conditions. Second, we develop several approximations of a population genetics model to show that the system exhibits different behaviours depending on the rate of migration. The main insights are the following: with intermediate migration, both genetic drift and migration decrease local adaptation; with low migration, drift decreases local adaptation but migration speeds up adaptation; with high migration, genetic drift has no effect on local adaptation. Third, we extend this analysis to cases where the trait under selection is continuous using classical quantitative genetics theory. Finally, we discuss these results in the light of recent experimental work on local adaptation.     

Impact of adaptation currents on synchronization of coupled exponential integrate-and-fire neurons

The ability of spiking neurons to synchronize their activity in a network depends on the response behavior of these neurons as quantified by the phase response curve (PRC) and on coupling properties. The PRC characterizes the effects of transient inputs on spike timing and can be measured experimentally. Here we use the adaptive exponential integrate-and-fire (aEIF) neuron model to determine how subthreshold and spike-triggered slow adaptation currents shape the PRC. Based on that, we predict how synchrony and phase locked states of coupled neurons change in presence of synaptic delays and unequal coupling strengths. We find that increased subthreshold adaptation currents cause a transition of the PRC from only phase advances to phase advances and delays in response to excitatory perturbations. Increased spike-triggered adaptation currents on the other hand predominantly skew the PRC to the right. Both adaptation induced changes of the PRC are modulated by spike frequency, being more prominent at lower frequencies. Applying phase reduction theory, we show that subthreshold adaptation stabilizes synchrony for pairs of coupled excitatory neurons, while spike-triggered adaptation causes locking with a small phase difference, as long as synaptic heterogeneities are negligible. For inhibitory pairs synchrony is stable and robust against conduction delays, and adaptation can mediate bistability of in-phase and anti-phase locking. We further demonstrate that stable synchrony and bistable in/anti-phase locking of pairs carry over to synchronization and clustering of larger networks. The effects of adaptation in aEIF neurons on PRCs and network dynamics qualitatively reflect those of biophysical adaptation currents in detailed Hodgkin-Huxley-based neurons, which underscores the utility of the aEIF model for investigating the dynamical behavior of networks. Our results suggest neuronal spike frequency adaptation as a mechanism synchronizing low frequency oscillations in local excitatory networks, but indicate that inhibition rather than excitation generates coherent rhythms at higher frequencies.     

Multiple mechanisms of spike-frequency adaptation in motoneurones.

Spike-frequency adaptation is the continuous decline in discharge rate in response to a constant stimulus. We have described three distinct phases of adaptation in rat hypoglossal motoneurones: initial, early and late. The initial phase of adaptation is over in one or two intervals, and is primarily due to summation of the calcium-activated potassium conductance underlying the medium duration afterhyperpolarization (mAHP). The biophysical mechanisms underlying the later phases of adaptation are not well understood. Two of the previously-proposed mechanisms for adaptation are an increase in outward current flowing through calcium-activated potassium channels and increasing outward current produced by the electrogenic sodium-potassium pump. We found that neither of these mechanisms are necessary for the expression of the early and late phases of adaptation. The magnitude of the initial phase of adaptation was reduced when the calcium in the external solution was replaced with manganese, but the magnitudes of the early and late phases were consistently increased under these conditions. Partial blockade of the sodium-potassium pump with ouabain had no significant effect on any of the three phases of adaptation. Our current working hypothesis is that the magnitude of late adaptation depends upon the interplay between slow inactivation of sodium currents, that tends to decrease discharge rate, and the slow activation or facilitation of a calcium current that tends to increase discharge rate. Adaptation is often associated with a progressive decrease in the peak amplitude and rate of rise of action potentials, and a computer model that incorporated slow inactivation of sodium channels reproduced this phenomenon. However, the time course of adaptation does not always parallel changes in spike shape, indicating that the progressive activation of another inward current might oppose the decline in frequency caused by slow sodium inactivation.     

Increased intracellular sodium mimics some but not all aspects of photoreceptor adaptation in the ventral eye of Limulus

The effects of the intracellular iontophoretic injection of Na+ ions have been quantitatively compared with adaptation in ventral photoreceptors of Limulus. We find that: (a) both light adaptation and sodium injection are associated with a decrease in the variability of the threshold response amplitued; (b) both light adaptation and sodium injection are associated with a decrease in the absolute value of the temporal dispersion of the threshold response time delay; (c) the same template curve adequately fits the intensity response relationships measured under light adaptation and Na+ injection; (d) both light adaptation and Na+ injection produce a fourfold decrease in response time delay for a desensitization of 3 log units; (e) the time coures of light adaptation and dark adaptation is significantly faster than the onset of and recovery from desensitization produced by Na+ injection; (f) unlike local illumination, Na+ injection does not produce localized desensitization of the photoreceptor. These findings suggest that a rise in intracellular Na+ concentration makes at most only a minor contribution (probably less than 5%) to the total adaptation of these receptors in the intensity range we have examined (up to 3 log units above absolute threshold). However, changes in intracellular Na+ concentration may contribute to certain components of light and dark adaptation in these receptors.     

A meta-analysis of factors affecting local adaptation between interacting species

Adaptive divergence among populations can result in local adaptation, whereby genotypes in native environments exhibit greater fitness than genotypes in novel environments. A body of theory has developed that predicts how different species traits, such as rates of gene flow and generation times, influence local adaptation in coevolutionary species interactions. We used a meta-analysis of local-adaptation studies across a broad range of host-parasite interactions to evaluate predictions about the effect of species traits on local adaptation. We also evaluated how experimental design influences the outcome of local adaptation experiments. In reciprocally designed experiments, the relative gene flow rate of hosts versus parasites was the strongest predictor of local adaptation, with significant parasite local adaptation only in the studies in which parasites had greater gene flow rates than their hosts. When nonreciprocal studies were included in analyses, species traits did not explain significant variation in local adaptation, although the overall level of local adaptation observed was lower in the nonreciprocal than in the reciprocal studies. This formal meta-analysis across a diversity of host-parasite systems lends insight into the role of both biology (species traits) and biologists (experimental design) in detecting local adaptation in coevolving species interactions.     

Sex, horizontal transmission, and multiple hosts prevent local adaptation of Crithidia bombi, a parasite of bumblebees (Bombus spp.)

Local adaptation within host-parasite systems can evolve by several non-exclusive drivers (e.g., host species-genetic adaptation; ecological conditions-ecological adaptation, and time-temporal adaptation). Social insects, especially bumblebees, with an annual colony life history not only provide an ideal system to test parasite transmission within and between different host colonies, but also parasite adaptation to specific host species and environments. Here, we study local adaptation in a multiple-host parasite characterized by high levels of horizontal transmission. Crithidia bombi occurs as a gut parasite in several bumblebee species. Parasites were sampled from five different host species in two subsequent years. Population genetic tools were used to test for the several types of adaptation. Although we found no evidence for local adaptation of the parasite toward host species, there was a slight temporal differentiation of the parasite populations, which might have resulted from severe bottlenecks during queen hibernation. Parasite populations were in Hardy-Weinberg equilibrium and showed no signs of linkage disequilibrium suggesting that sexual reproduction is an alternative strategy in this otherwise clonal parasite. Moreover, high levels of multiple infections were found, which might facilitate sexual genetic exchange. The detection of identical clones in different host species suggested that horizontal transmission occurs between host species and underpins the lack of host-specific adaptation.     

Awareness of Sensorimotor Adaptation to Visual Rotations of Different Size

Previous studies on sensorimotor adaptation revealed no awareness of the nature of the perturbation after adaptation to an abrupt 30° rotation of visual feedback or after adaptation to gradually introduced perturbations. Whether the degree of awareness depends on the magnitude of the perturbation, though, has as yet not been tested. Instead of using questionnaires, as was often done in previous work, the present study used a process dissociation procedure to measure awareness and unawareness. A naïve, implicit group and a group of subjects using explicit strategies adapted to 20°, 40° and 60° cursor rotations in different adaptation blocks that were each followed by determination of awareness and unawareness indices. The awareness index differed between groups and increased from 20° to 60° adaptation. In contrast, there was no group difference for the unawareness index, but it also depended on the size of the rotation. Early adaptation varied between groups and correlated with awareness: The more awareness a participant had developed the more the person adapted in the beginning of the adaptation block. In addition, there was a significant group difference for savings but it did not correlate with awareness. Our findings suggest that awareness depends on perturbation size and that aware and strategic processes are differentially involved during adaptation and savings. Moreover, the use of the process dissociation procedure opens the opportunity to determine awareness and unawareness indices in future sensorimotor adaptation research.     

Steady State of Photosynthesis in Cyanobacterial Photosynthetic Systems Before and After Regulation of Electron Transport Composition: Overall Rate of Photosynthesis and PSI/PS II Composition

The effect of regulation of photosystem (PS) composition onthe photosynthetic steady state was examined using the cyanobacteriumSynechocystis PCC 6714. Photosynthetic rates under orange lightabsorbed by phycobiliprotein (PBP) (PBP light) and under redlight absorbed mainly by chlorophyll a (Chi a light) were comparedfor the cells before and after adaptation to the respectivelight regimes. Results were as follows: (1) Photosynthetic ratesper absorbed light quantum became higher after adaptation thanthose before adaptation. (2) Under Chi a light, the low turnoverrate of PS I before adaptation was markedly enhanced after adaptation(decrease in PS I content), but in the case of adaptation toPBP light (increase in PS I content), a marked enhancement ofPS II turnover occurred after adaptation. (3) In the formercase, a low turnover rate of PS I before adaptation was dueto the occurrence of a large number of closed PS I complexes,but in the latter, limited excitation of PS I caused a largenumber of closed PS II complexes before adaptation. Resultsfor the latter case indicate that the energy transfer from phycobilisome(PBS) to one PS I complex is far smaller than that from PBSto one PS II complex, and that the imbalance of energy distributionfrom PBS to the two photosystems is compensated for by the increasein the number of PS I complexes. (Received September 10, 1987; Accepted December 9, 1987)     

Comparative evaluation of the protective effect of adaptation to short-term stress exposures in damage to the heart and portal vein from long-term stress

The effect of the preliminary adaptation to short-term stress actions carried out under different conditions was studied in the myocardium and vascular smooth muscle damaged by long-term immobilization stress. The preliminary adaptation performed under "sparing" conditions was shown to protect more effectively the right atrial myocardium and portal vein against damages induced by long-term immobilization than that carried out under stringent conditions. The sparing adaptation allowed avoiding the appearance of the structural "price" of the adaptation, i.e. the depression of myocardial contractile function induced by adaptation itself.