Evolutionary theory predicts an interactive process whereby spatiotemporal environmental heterogeneity will maintain genetic variation, while genetic and phenotypic diversity will buffer populations against stress and allow for fast adaptive evolution in rapidly changing environments. Here, we study color polymorphism patterns in pygmy grasshoppers (Tetrix subulata) and show that the frequency of the melanistic (black) color variant was higher in areas that had been ravaged by fires the previous year than in nonburned habitats, that, in burned areas, the frequency of melanistic grasshoppers dropped from ca. 50% one year after a fire to 30% after four years, and that the variation in frequencies of melanistic individuals among and within populations An improved knowledge of how environmental change affects natural populations of plants and animals is crucial for our understanding of evolution of biological diversity as well as for the development of successful plans for protection and management of biodiversity (Hanski 1998;Lande 1998;Bell 2010). The influence of natural selection on biodiversity in unstable and heterogeneous environments has been debated since the middle of the 20th century. Theory posits that overall, spatially divergent selection in combination with gene flow generally provides broad conditions for maintenance of genetic polymorphism and that fluctuating selection in temporally changing environments may maintain genetic variation under restricted conditions, but the consequences are scale dependent. The effect of spatial variation depends on if the environment is fine or coarse grained relative to the dispersal capacity of the organism, and whether temporally changing environments will promote or erode genetic variation depends on the frequency of change relative to the life span of the organism and on whether generations are overlapping or discrete (Haldane and
BackgroundAnimal colour patterns offer good model systems for studies of biodiversity and evolution of local adaptations. An increasingly popular approach to study the role of selection for camouflage for evolutionary trajectories of animal colour patterns is to present images of prey on paper or computer screens to human ‘predators’. Yet, few attempts have been made to confirm that rates of detection by humans can predict patterns of selection and evolutionary modifications of prey colour patterns in nature. In this study, we first analyzed encounters between human ‘predators’ and images of natural black, grey and striped colour morphs of the polymorphic Tetrix subulata pygmy grasshoppers presented on background images of unburnt, intermediate or completely burnt natural habitats. Next, we compared detection rates with estimates of capture probabilities and survival of free-ranging grasshoppers, and with estimates of relative morph frequencies in natural populations.ResultsThe proportion of grasshoppers that were detected and time to detection depended on both the colour pattern of the prey and on the type of visual background. Grasshoppers were detected more often and faster on unburnt backgrounds than on 50% and 100% burnt backgrounds. Striped prey were detected less often than grey or black prey on unburnt backgrounds; grey prey were detected more often than black or striped prey on 50% burnt backgrounds; and black prey were detected less often than grey prey on 100% burnt backgrounds. Rates of detection mirrored previously reported rates of capture by humans of free-ranging grasshoppers, as well as morph specific survival in the wild. Rates of detection were also correlated with frequencies of striped, black and grey morphs in samples of T. subulata from natural populations that occupied the three habitat types used for the detection experiment.ConclusionsOur findings demonstrate that crypsis is background-dependent, and implicate visual predation as an important driver of evolutionary modifications of colour polymorphism in pygmy grasshoppers. Our study provides the clearest evidence to date that using humans as ‘predators’ in detection experiments may provide reliable information on the protective values of prey colour patterns and of natural selection and microevolution of camouflage in the wild.
The existence of melanistic (black) color forms in many species represents interesting model systems that have played important roles for our understanding of selective processes, evolution of adaptations, and the maintenance of variation. A recent study reported on rapid evolutionary shifts in frequencies of the melanistic forms in replicated populations of Tetrix subulata pygmy grasshoppers; the incidence of the melanistic form was higher in recently burned areas with backgrounds blackened by fire than in nonburned areas, and it declined over time in postfire environments. Here, we tested the hypothesis that the frequency shifts of the black color variant were driven, at least in part, by changes in the selective regime imposed by visual predators. To study detectability of the melanistic form, we presented human “predators” with images of black grasshoppers and samples of the natural habitat on computer screens. We demonstrate that the protective value of black coloration differs between burnt and nonburnt environments and gradually increases in habitats that have been more blackened by fire. These findings support the notion that a black color pattern provides improved protection from visually oriented predators against blackened backgrounds and implicate camouflage and predation as important drivers of fire melanism in pygmy grasshoppers.
Polymorphism, the coexistence of two or more variants within a population, has served as a classic model system to address questions about the evolution and maintenance of intraspecific variation. It has been hypothesized that a natural level of colour polymorphism may impair the search efficiency of visually orientated predators. To test this polymorphism protects hypothesis, we asked human participants to search for images of natural black, striped or grey Tetrix subulata grasshopper colour morphs presented against photographs of their natural habitat on computer screens. Fewer grasshoppers were detected when morphs were presented in mixed than in uniform sequences. All three morphs benefited to comparable degrees, in terms of reduced detection, from being presented in polymorphic sequences. Our findings demonstrate that natural levels of polymorphic variation can impede the efficiency of visually orientated predators and increase survival of prey. This protective effect supports the limited attention hypothesis, explains why predators develop 'search images', may account for the spread and establishment of novel colour variants, and contributes to maintenance of polymorphisms.
Gene flow is often regarded a random process that homogenizes differences between populations and constrains local adaptation. However, the matching habitat choice hypothesis posits that individuals actively choose those microhabitats that best match their specific phenotype to maximize fitness. Dispersal (and possibly gene flow) may thus be directed. Many studies report associations between habitats and phenotypes, but they may reflect selection, plasticity or adaptation rather than matching choice. Here, we test two predictions from the matching habitat choice hypothesis by manipulating the dorsal colour of Tetrix subulata, a pygmy grasshopper. (1) Is microhabitat choice flexible such that differently manipulated phenotypes distribute themselves differently in a microclimatic and solar radiation mosaic? (2) If they do, are their fitness prospects higher in the more preferred microhabitat? We find that individuals painted white or black do distribute themselves differently, with black individuals residing in habitats with less radiation, on average, than white individuals, demonstrating that microhabitat choices are plastic. Furthermore, white females had more hatchlings than black ones in the increased radiation treatment, and this was mainly due to increased mortality of black females under increased radiation. These findings provide rare experimental evidence in line with predictions from the matching habitat choice hypothesis.
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