Artificial Selection Experiments Research Articles

Heritability and artificial selection on ambulatory dispersal distance in Tetranychus urticae: effects of density and maternal effects.

Dispersal distance is understudied although the evolution of dispersal distance affects the distribution of genetic diversity through space. Using the two-spotted spider mite, Tetranychus urticae, we tested the conditions under which dispersal distance could evolve. To this aim, we performed artificial selection based on dispersal distance by choosing 40 individuals (out of 150) that settled furthest from the home patch (high dispersal, HDIS) and 40 individuals that remained close to the home patch (low dispersal, LDIS) with three replicates per treatment. We did not observe a response to selection nor a difference between treatments in life-history traits (fecundity, survival, longevity, and sex-ratio) after ten generations of selection. However, we show that heritability for dispersal distance depends on density. Heritability for dispersal distance was low and non-significant when using the same density as the artificial selection experiments while heritability becomes significant at a lower density. Furthermore, we show that maternal effects may have influenced the dispersal behaviour of the mites. Our results suggest primarily that selection did not work because high density and maternal effects induced phenotypic plasticity for dispersal distance. Density and maternal effects may affect the evolution of dispersal distance and should be incorporated into future theoretical and empirical studies.

The evolution of endothermy in Cenozoic mammals: a plesiomorphic‐apomorphic continuum

The evolution of endothermy in birds and mammals was one of the most important events in the evolution of the vertebrates. Past tests of hypotheses on the evolution of endothermy in mammals have relied largely on analyses of the relationship between basal and maximum metabolic rate, and artificial selection experiments. I argue that components of existing hypotheses, as well as new hypotheses, can be tested using an alternative macrophysiological modeling approach by examining the development of endothermy during the Cenozoic. Recent mammals display a 10°C range in body temperature which is sufficiently large to identify the selective forces that have driven the development of endothermy from a plesiomorphic (ancestral) Cretaceous or Jurassic condition. A model is presented (the Plesiomorphic-Apomorphic Endothermy Model, PAE Model) which proposes that heterothermy, i.e. bouts of normothermy (constant body temperature) interspersed with adaptive heterothermy (e.g. daily torpor and/or hibernation), was the ancestral condition from which apomorphic (derived), rigid homeothermy evolved. All terrestrial mammal lineages are examined for existing data to test the model, as well as for missing data that could be used to test the model. With the exception of Scandentia and Dermoptera, about which little is known, all mammalian orders that include small-sized mammals (<500 g), have species which are heterothermic and display characteristics of endothermy which fall somewhere along a plesiomorphic-apomorphic continuum. Orders which do not have heterothermic representatives (Cetartiodactyla, Perissodactyla, Pholidota, and Lagomorpha) are comprised of medium- to large-sized mammals that have either lost the capacity for heterothermy, or in which heterothermy has yet to be measured. Mammalian heterothermy seems to be plesiomorphic and probably evolved once in the mammalian lineage. Several categories of endothermy are identified (protoendothermy, plesioendothermy, apoendothermy, basoendothermy, mesoendothermy, supraendothermy, and reversed mesoendothermy) to describe the evolution of endothermy during the Cenozoic. The PAE Model should facilitate the testing of hypotheses using a range of macrophysiological methods (e.g. the comparative method and the reconstruction of ancestral states).

Flyway evolution is too fast to be explained by the modern synthesis: proposals for an ‘extended’ evolutionary research agenda

In this paper, I argue that to fully grasp the generation and maintenance of variation in the migratory phenotypes of (shore-)birds we need to expand our scientific search image and include developmental processes and non-genetic pathways of inheritance in the explanatory frameworks. Traditionally, studies of micro-evolution of migratory phenotypes were restricted to comparative studies on migratory versus non-migratory taxa, and artificial selection and heritability experiments on quantitative behavioural traits related to migration. Such studies had a focus on the genetic axis of inheritance and were restricted to songbirds. In avian groups such as the shorebird families Scolopacidae and Charadriidae, all but a few island species are migrants, which precludes comparative studies at the species level. Like other taxa, shorebirds have geographically separate breeding populations (either or not recognized as subspecies on the basis of morphological differences) which differentiate with respect to the length, general direction and timing of migration, including the use of fuelling at staging sites and the timing of moult. However, their breeding systems preclude artificial selection and heritability experiments on quantitative traits. This would seem to limit the prospects of evolutionary analysis until one realizes that the speed of evolutionary innovation in shorebird migratory life-histories may be so fast as to necessitate other avenues of explanation and investigation. According to our best current estimates based on mitochondrial gene sequence variation, in Red Knots Calidris canutus considerable phenotypic variation has evolved since the Last Glacial Maximum ca. 20,000 years ago, to the extent that six subspecies are currently recognized. This would be too short a time for the origin of the qualitatively and quantitatively distinct and non-overlapping traits to be explained by random point mutations followed by natural selection, although we cannot dismiss the possibility of previously unexpressed (standing) genetic variation followed by selection. I argue that, to understand the flyway evolution of such shorebirds in the ‘extended’ evolutionary framework, we need to give due attention to developmental versatility and broad-sense epigenetic evolutionary mechanisms. This means that experimental studies at the phenotypic level are now necessary. This could involve a combination of observational studies in our rapidly changing world, common garden experiments, and even experiments involving global-scale displacements of particular migratory phenotypes at different phases of development. I provide suggestions on how such experiments could be carried out.

Microbial Communities as Experimental Units

Artificial ecosystem selection is an experimental technique that treats microbial communities as though they were discrete units by applying selection on community-level properties. Highly diverse microbial communities associated with humans and other organisms can have significant impacts on the health of the host. It is difficult to find correlations between microbial community composition and community-associated diseases, in part because it may be impossible to define a universal and robust species concept for microbes. Microbial communities are composed of potentially thousands of unique populations that evolved in intimate contact, so it is appropriate in many situations to view the community as the unit of analysis. This perspective is supported by recent discoveries using metagenomics and pangenomics. Artificial ecosystem selection experiments can be costly, but they bring the logical rigor of biological model systems to the emerging field of microbial community analysis.

Rapid gain and loss of evolutionary resistance to the harmful dinoflagellate Cochlodinium polykrikoides in the copepod Acartia tonsa

Evolutionary resistance of the copepod Acartia tonsa to the dinoflagellate Cochlodinium polykrikoides was investigated to establish whether zooplankton can rapidly adapt to harmful algal blooms (HABs). Copepod resistance was evaluated by egg production rates when feeding on C. polykrikoides relative to the nontoxic flagellate Rhodomonas lens. An experiment with six geographically separate A. tonsa populations demonstrated that the copepods collected during C. polykrikoides blooms within eastern Long Island bays were significantly more resistant to C. polykrikoides than their conspecifics in nearby nonbloom regions. An artificial selection experiment with a naïve A. tonsa population demonstrated that copepod resistance significantly increased when individuals were chronically exposed to C. polykrikoides (three times greater than the control after four generations). Following a two‐generation relaxation of selection, however, the elevated resistance in A. tonsa was completely lost. Such rapid gain and loss of resistance suggests that copepod adaptation to C. polykrikoides in the bays of eastern Long Island may mainly result from the selection of resistant genotypes by an ongoing bloom event rather than prior HABs, which could shape trophic interactions between zooplankton and harmful algae.

The molecular genetics of clinal variation: a case study of ebony and thoracic trident pigmentation in Drosophila melanogaster from eastern Australia

Widespread pigmentation diversity coupled with a well-defined genetic system of melanin synthesis and patterning in Drosophila provides an excellent opportunity to study phenotypes undergoing evolutionary change. Pigmentation variation is highly correlated with different ecological variables and is thought to reflect adaptations to different environments. Several studies have linked candidate genes from Drosophila melanogaster to intra-population variation and interspecific morphological divergence, but less clearly to variation among populations forming pigmentation clines. We characterized a new thoracic trident pigmentation cline in D. melanogaster populations from eastern Australia, and applied a candidate gene approach to explain the majority of the geographically structured phenotypic variation. More melanized populations from higher latitudes tended to express less ebony than their tropical counterparts, and an independent artificial selection experiment confirmed this association. By partitioning temperature dependent effects, we showed that the genetic differences underlying clinal patterns for trident variation at 25 °C do not explain the patterns observed at 16 °C. Changes in thoracic trident pigmentation could be a common evolutionary response to climatically mediated environmental pressures. On the Australian east coast most of the changes appear to be associated with regulatory divergence of the ebony gene but this depends on temperature.

Natural selection stops the evolution of male attractiveness

Sexual selection in natural populations acts on highly heritable traits and tends to be relatively strong, implicating sexual selection as a causal agent in many phenotypic radiations. Sexual selection appears to be ineffectual in promoting phenotypic divergence among contemporary natural populations, however, and there is little evidence from artificial selection experiments that sexual fitness can evolve. Here, we demonstrate that a multivariate male trait preferred by Drosophila serrata females can respond to selection and results in the maintenance of male mating success. The response to selection was associated with a gene of major effect increasing in frequency from 12 to 35% in seven generations. No further response to selection, or increase in frequency of the major gene, was observed between generations 7 and 11, indicating an evolutionary limit had been reached. Genetic analyses excluded both depletion of genetic variation and overdominance as causes of the evolutionary limit. Relaxing artificial selection resulted in the loss of 52% of the selection response after a further five generations, demonstrating that the response under artificial sexual selection was opposed by antagonistic natural selection. We conclude that male D. serrata sexually selected traits, and attractiveness to D. serrata females conferred by these traits, were held at an evolutionary limit by the lack of genetic variation that would allow an increase in sexual fitness while simultaneously maintaining nonsexual fitness. Our results suggest that sexual selection is unlikely to cause divergence among natural populations without a concomitant change in natural selection, a conclusion consistent with observational evidence from natural populations.

Ambulatory dispersal in Tetranychus urticae: an artificial selection experiment on propensity to disperse yields no response

Dispersal to new hosts is an important process for an invasive herbivore, such as the two-spotted spider mite. A recent study, using artificial selection experiments, has suggested that genetic variation and genetic trade-offs are present for propensity to disperse in this species. However, due to the experimental setup alternative explanations for the response to selection could not be ruled out. Using an altered setup, we investigated whether the propensity for ambulatory dispersal differs genetically between individuals and whether genetic correlations with life-history traits exist. Upward and downward selection on propensity to leave the colony was performed for seven generations in four replicate artificial selection experiments and the results were compared to control lines. No consistent responses to selection were found and no significant effect on life-history traits (oviposition rate, juvenile survival, development rate and number of adult offspring) or sex ratio was present across the replicates. The data suggest that our base population of spider mites harbours at best a low amount of additive genetic variation for this behaviour.Electronic supplementary materialThe online version of this article (doi:10.1007/s10493-010-9411-7) contains supplementary material, which is available to authorized users.

LIFE HISTORY VARIATION IN AN ARTIFICIALLY SELECTED POPULATION OF DROSOPHILA MELANOGASTER: PLEIOTROPY, SUPERFLIES, AND AGE-SPECIFIC ADAPTATION

We measured age-specific fecundity and survival in recombinant inbred lines of Drosophila melanogaster that were derived from an artificial selection experiment for delayed reproduction. Age at peak oviposition is highly heritable (h(2) (B) = 0.55). We find three qualitative categories of peak oviposition: early-, midlife-, and bimodal. Genetic correlations between life span and early fecundity are not significantly different from zero, but correlations with midlife fecundity are positive and statistically significant. Long-lived genotypes exhibit a midlife fecundity peak. There is no evidence for a shift of reproductive effort from early to later stages. The existence of qualitatively recombinant phenotypes, including "superflies" that exhibit both enhanced survival and high levels of early fecundity, argues against the widespread idea that life history evolution in Drosophila is dominated by negative pleiotropy. There is clear evidence of age-specific adaptation in the timing of oviposition.

Global change and the evolution of phenotypic plasticity in plants

Global change drivers create new environmental scenarios and selective pressures, affecting plant species in various interacting ways. Plants respond with changes in phenology, physiology, and reproduction, with consequences for biotic interactions and community composition. We review information on phenotypic plasticity, a primary means by which plants cope with global change scenarios, recommending promising approaches for investigating the evolution of plasticity and describing constraints to its evolution. We discuss the important but largely ignored role of phenotypic plasticity in range shifts and review the extensive literature on invasive species as models of evolutionary change in novel environments. Plasticity can play a role both in the short-term response of plant populations to global change as well as in their long-term fate through the maintenance of genetic variation. In new environmental conditions, plasticity of certain functional traits may be beneficial (i.e., the plastic response is accompanied by a fitness advantage) and thus selected for. Plasticity can also be relevant in the establishment and persistence of plants in novel environments that are crucial for populations at the colonizing edge in range shifts induced by climate change. Experimental studies show taxonomically widespread plastic responses to global change drivers in many functional traits, though there is a lack of empirical support for many theoretical models on the evolution of phenotypic plasticity. Future studies should assess the adaptive value and evolutionary potential of plasticity under complex, realistic global change scenarios. Promising tools include resurrection protocols and artificial selection experiments.

Rapid evolution of cold tolerance in stickleback

Climate change is predicted to lead to increased average temperatures and greater intensity and frequency of high and low temperature extremes, but the evolutionary consequences for biological communities are not well understood. Studies of adaptive evolution of temperature tolerance have typically involved correlative analyses of natural populations or artificial selection experiments in the laboratory. Field experiments are required to provide estimates of the timing and strength of natural selection, enhance understanding of the genetics of adaptation and yield insights into the mechanisms driving evolutionary change. Here, we report the experimental evolution of cold tolerance in natural populations of threespine stickleback fish (Gasterosteus aculeatus). We show that freshwater sticklebacks are able to tolerate lower minimum temperatures than marine sticklebacks and that this difference is heritable. We transplanted marine sticklebacks to freshwater ponds and measured the rate of evolution after three generations in this environment. Cold tolerance evolved at a rate of 0.63 haldanes to a value 2.5°C lower than that of the ancestral population, matching values found in wild freshwater populations. Our results suggest that cold tolerance is under strong selection and that marine sticklebacks carry sufficient genetic variation to adapt to changes in temperature over remarkably short time scales.

Current selection for lower migratory activity will drive the evolution of residency in a migratory bird population

Global warming is impacting biodiversity by altering the distribution, abundance, and phenology of a wide range of animal and plant species. One of the best documented responses to recent climate change is alterations in the migratory behavior of birds, but the mechanisms underlying these phenotypic adjustments are largely unknown. This knowledge is still crucial to predict whether populations of migratory birds will adapt to a rapid increase in temperature. We monitored migratory behavior in a population of blackcaps (Sylvia atricapilla) to test for evolutionary responses to recent climate change. Using a common garden experiment in time and captive breeding we demonstrated a genetic reduction in migratory activity and evolutionary change in phenotypic plasticity of migration onset. An artificial selection experiment further revealed that residency will rapidly evolve in completely migratory bird populations if selection for shorter migration distance persists. Our findings suggest that current alterations of the environment are favoring birds wintering closer to the breeding grounds and that populations of migratory birds have strongly responded to these changes in selection. The reduction of migratory activity is probably an important evolutionary process in the adaptation of migratory birds to climate change, because it reduces migration costs and facilitates the rapid adjustment to the shifts in the timing of food availability during reproduction.

The action of evolutionary forces on metric traits

Fisher's theorem of natural selection implies that the population genetic variance of quasi-neutral traits should be mostly additive. In the case of fitness component traits, however, that variance would be characterised by a substantial contribution from non-additive loci. In parallel, Robertson's theorem states that selection will change the population mean of a trait proportionally to the magnitude of the genetic correlation between that trait and fitness, which should be weak for quasi-neutral traits or strong for the mean fitness components. Drosophila data from inbreeding and artificial selection experiments are discussed within that theoretical framework. In addition, the process of regeneration by mutation of the genetic variance of a quasi-neutral trait (abdominal bristle number) in a Drosophila population initially homozygous at all loci has been analysed. After 485 generations of mutation accumulation, the levels of additive variance found in this population closely approached those commonly observed in laboratory populations. Furthermore, these values, together with previously reported estimates for natural populations, could be jointly explained by a model assuming weak causal stabilising selection.

Estimating genetic architectures from artificial-selection responses: A random-effect framework

Artificial-selection experiments on plants and animals generate large datasets reporting phenotypic changes in the course of time. The dynamics of the changes reflect the underlying genetic architecture, but only simple statistical tools have so far been available to analyze such time series. This manuscript describes a general statistical framework based on random-effect models aiming at estimating key parameters of genetic architectures from artificial-selection responses. We derive explicit Mendelian models (in which the genetic architecture relies on one or two large-effect loci), and compare them with classical polygenic models. With simulations, we show that the models are accurate and powerful enough to provide useful estimates from realistic experimental designs, and we demonstrate that model selection is effective in picking few-locus vs. polygenic genetic architectures even from medium-quality artificial-selection data. The method is illustrated by the analysis of a historical selection experiment, carried on color pattern in rats by Castle et al.

Natural and artificial RNAs occupy the same restricted region of sequence space

Different chemical and mutational processes within genomes give rise to sequences with different compositions and perhaps different capacities for evolution. The evolution of functional RNAs may occur on a "neutral network" in which sequences with any given function can easily mutate to sequences with any other. This neutral network hypothesis is more likely if there is a particular region of composition that contains sequences that are functional in general, and if many different functions are possible within this preferred region of composition. We show that sequence preferences in active sites recovered by in vitro selection combine with biophysical folding rules to support the neutral network hypothesis. These simple active-site specifications and folding preferences obtained by artificial selection experiments recapture the previously observed purine bias and specific spread along the GC axis of naturally occurring aptamers and ribozymes isolated from organisms, although other types of RNAs, such as miRNA precursors and spliceosomal RNAs, that act primarily through complementarity to other amino acids do not share these preferences. These universal evolved sequence features are therefore intrinsic in RNA molecules that bind small-molecule targets or catalyze reactions.

Heritability of Directional Asymmetry inDrosophila melanogaster

Directional asymmetry (DA), the consistent difference between a pair of morphological structures in which the same side is always larger than the other, presents an evolutionary mystery. Although many paired traits show DA, genetic variation for DA has not been unambiguously demonstrated. Artificial selection is a powerful technique for uncovering selectable genetic variation; we review and critique the limited number of previous studies that have been performed to select on DA and present the results of a novel artificial selection experiment on the DA of posterior crossvein location in Drosophila wings. Fifteen generations of selection in two genetically distinct lines were performed and none of the lines showed a significant response to selection. Our results therefore support and reconfirm previous findings; despite apparent natural variation and evolution of DA in nature, DA remains a paradoxical trait that does not respond to artificial selection.

Life-history traits and energetic status in relation to vulnerability to angling in an experimentally selected teleost fish.

In recreational fisheries, a correlation has been established between fishing-induced selection pressures and the metabolic traits of individual fish. This study used a population of largemouth bass (Micropterus salmoides) with lines of low vulnerability fish (LVF) and high vulnerability fish (HVF) that were previously established through artificial truncation selection experiments. The main objective was to evaluate if differential vulnerability to angling was correlated with growth, energetics and nutritional condition during the sub-adult stage. Absolute growth rate was found to be between 9% and 17% higher for LVF compared with HVF over a 6-month period in three experimental ponds. The gonadosomatic index in females was lower for LVF compared with HVF in one experimental pond. No significant differences in energy stores (measured using body constituent analysis) were observed between LVF and HVF. In addition, both groups were consuming the same prey items as evidenced by stomach content analysis. The inherent reasons behind differential vulnerability to angling are complex, and selection for these opposing phenotypes appears to select for differing growth rates, although the driving factors remain unclear. These traits are important from a life-history perspective, and alterations to their frequency as a result of fishing-induced selection could alter fish population structure. These findings further emphasize the need to incorporate evolutionary principles into fisheries management activities.

Laboratory model of adaptive radiation: Activity and metabolic rates in bank voles from a multidirectional artificial selection experiment

Laboratory model of adaptive radiation: Activity and metabolic rates in bank voles from a multidirectional artificial selection experiment

What can genetic variation tell us about the evolution of senescence?

Quantitative genetic approaches have been developed that allow researchers to determine which of two mechanisms, mutation accumulation (MA) or antagonistic pleiotropy (AP), best explain observed variation in patterns of senescence using classical quantitative genetic techniques. These include the creation of mutation accumulation lines, artificial selection experiments and the partitioning of genetic variances across age classes. This last strategy has received the lion's share of empirical attention. Models predict that inbreeding depression (ID), dominance variance and the variance among inbred line means will all increase with age under MA but not under those forms of AP that generate marginal overdominance. Here, we show that these measures are not, in fact, diagnostic of MA versus AP. In particular, the assumptions about the value of genetic parameters in existing AP models may be rather narrow, and often violated in reality. We argue that whenever ageing-related AP loci contribute to segregating genetic variation, polymorphism at these loci will be enhanced by genetic effects that will also cause ID and dominance variance to increase with age, effects also expected under the MA model of senescence. We suggest that the tests that seek to identify the relative contributions of AP and MA to the evolution of ageing by partitioning genetic variance components are likely to be too conservative to be of general value.

Does artificial selection on diapause incidence cause correlational changes in other life‐history traits? Case study in a spider mite population

AbstractTheoretical studies suggest that the timing of entering hibernation by arthropods has large effects on long‐term fitness, incurring strong selection pressure on diapause attributes every year. On the other hand, diapause attributes are often genetically correlated with other important life‐history traits such as fecundity or development time. To understand the evolutionary process of life cycle formation, there is a need to investigate not only diapause attributes themselves but also their genetic association with other life‐history traits. The Kanzawa spider mite, Tetranychus kanzawai Kishida (Acari: Tetranychidae), is a small herbivore that lives on the undersurface of host plant leaves. This mite has been investigated for the mode of inheritance of diapause attributes, but scarcely for genetic correlations with other life‐history traits. Here, I investigated whether diapause proneness, measured as the proportion of diapausing females under short‐day conditions, is genetically correlated with fecundity or development time under long‐day conditions using artificial selection experiments. Diapause incidence responded to the selection for both increasing and decreasing directions, suggesting that high genetic variance in diapause proneness is maintained in the study population. However, the change in proportion of diapausing females during the selection period was not associated with responses in fecundity or development time. These results suggest that diapause proneness and other life‐history traits have different genetic backgrounds, and thus diapause proneness may freely evolve without being constrained by changes in other life‐history traits.