Non-adaptive Phenotypic Plasticity Research Articles

Hatching phenology is lagging behind an advancing snowmelt pattern in a high-alpine bird

To track peaks in resource abundance, temperate-zone animals use predictive environmental cues to rear their offspring when conditions are most favourable. However, climate change threatens the reliability of such cues when an animal and its resource respond differently to a changing environment. This is especially problematic in alpine environments, where climate warming exceeds the Holarctic trend and may thus lead to rapid asynchrony between peaks in resource abundance and periods of increased resource requirements such as reproductive period of high-alpine specialists. We therefore investigated interannual variation and long-term trends in the breeding phenology of a high-alpine specialist, the white-winged snowfinch, Montifringilla nivalis, using a 20-year dataset from Switzerland. We found that two thirds of broods hatched during snowmelt. Hatching dates positively correlated with April and May precipitation, but changes in mean hatching dates did not coincide with earlier snowmelt in recent years. Our results offer a potential explanation for recently observed population declines already recognisable at lower elevations. We discuss non-adaptive phenotypic plasticity as a potential cause for the asynchrony between changes in snowmelt and hatching dates of snowfinches, but the underlying causes are subject to further research.

Nests in the cities: adaptive and non-adaptive phenotypic plasticity and convergence in an urban bird

Phenotypic plasticity plays a critical role in adaptation to novel environments. Behavioural plasticity enables more rapid responses to unfamiliar conditions than evolution by natural selection. Urban ecosystems are one such novel environment in which behavioural plasticity has been documented. However, whether such plasticity is adaptive, and if plasticity is convergent among urban populations, is poorly understood. We studied the nesting biology of an ‘urban-adapter’ species, the dark-eyed junco ( Junco hyemalis ), to understand the role of plasticity in adapting to city life. We examined (i) whether novel nesting behaviours are adaptive, (ii) whether pairs modify nest characteristics in response to prior outcomes, and (iii) whether two urban populations exhibit similar nesting behaviour. We monitored 170 junco nests in urban Los Angeles and compared our results with prior research on 579 nests from urban San Diego. We found that nests placed in ecologically novel locations (off-ground and on artificial surfaces) increased fitness, and that pairs practiced informed re-nesting in site selection. The Los Angeles population more frequently nested off-ground than the San Diego population and exhibited a higher success rate. Our findings suggest that plasticity facilitates adaptation to urban environments, and that the drivers behind novel nesting behaviours are complex and multifaceted.

Phenotypic plasticity, global change, and the speed of adaptive evolution.

The role phenotypic plasticity might play in adaptation to the ongoing climate changes is unclear. Plasticity allows for the production of a diversity of intra-generational responses, whose inter-generational evolutionary consequences are difficult to predict. In this article, we review theory and empirical studies addressing this question in insects by considering three scenarios. The first scenario corresponds to adaptive plasticity that should lead to slow or no evolution. The second scenario is the case of non-adaptive phenotypic plasticity to new environmental conditions that should lead either to extinction or, on the contrary, to rapid evolutionary change. The third scenario deals with how plasticity alters the variance selection acts upon. These scenarios are then discussed by highlighting examples of empirical studies on insects. We conclude that more studies are needed to better understand the relationship between phenotypic plasticity and evolutionary processes in insects.

Phenotypic plasticity of Artemisia ordosica seedlings in response to different levels of calcium carbonate in soil

Plant phenotypic plasticity is a common feature that is crucial for explaining interspecific competition, dynamics and biological evolution of plant communities. In this study, we tested the effects of soil CaCO3 (calcium carbonate) on the phenotypic plasticity of a psammophyte, Artemisia ordosica, an important plant species on sandy lands in arid and semi-arid areas of China, by performing pot experiments under different CaCO3 contents with a two-factor randomized block design and two orthogonal designs. We analyzed the growth responses (including plant height, root length, shoot-leaf biomass and root biomass) of A. ordosica seedlings to different soil CaCO3 contents. The results revealed that, with a greater soil CaCO3 content, A. ordosica seedlings gradually grew more slowly, with their relative growth rates of plant height, root length, shoot-leaf biomass and root biomass all decreasing significantly. Root N/P ratios showed significant negative correlations with the relative growth rates of plant height, shoot-leaf biomass and root length of A. ordosica seedlings; however, the relative growth rate of root length increased significantly with the root P concentration increased, showing a positive correlation. These results demonstrate that soil CaCO3 reduces the local P availability in soil, which produces a non-adaptive phenotypic plasticity to A. ordosica seedlings. This study should prove useful for planning and promoting the restoration of damaged/degraded vegetation in arid and semi-arid areas of China.

Heritability of behavioural tolerance to high CO2 in a coral reef fish is masked by nonadaptive phenotypic plasticity.

Previous studies have demonstrated limited potential for acclimation of adversely affected olfactory behaviours in reef fishes under elevated CO 2, indicating that genetic adaptation will be required to maintain behavioural performance in the future. Adaptation depends on the presence of heritable phenotypic variation in the trait, which may differ between populations and environments. We used parent–offspring regressions to estimate the heritability (h 2) of variation in behavioural tolerance to high CO 2 (754 μatm) in both field‐collected and laboratory‐reared families of Acanthochromis polyacanthus. Tolerance to elevated CO 2 was measured by determining the behavioural response of individuals to chemical alarm cues. Both populations exhibited high heritability of olfactory behaviour phenotype (father–mid‐offspring h 2 = 0.56 & 0.65, respectively) when offspring were acutely exposed to high CO 2 for 4 days. However, there was no heritability in the behavioural phenotype when juveniles were chronically exposed to high CO 2 for 6 weeks in the laboratory‐reared families. Parental exposure to high CO 2 during the breeding season did not alter this relationship between heritability and length of juvenile exposure to high CO 2. These results demonstrate that variation in behavioural tolerance to high CO 2 is heritable, but adaptive potential may be constrained by a loss of phenotypic variation when juveniles permanently experience a high‐CO 2 environment, as will occur with rising CO 2 levels in the ocean.

Evolutionary role of phenotypic plasticity

Phenotypic plasticity, i.e., the ability of a genotype to produce various phenotypes in response to changes in the environment, plays an important, although poorly understood and often underestimated, role in evolution. Both adaptive and nonadaptive phenotypic plasticity modulate the strength and direction of selection acting on a population and can, depending on conditions, either accelerate or inhibit adaptation, divergence, and speciation. Phenotypic plasticity also affects the direction of evolutionary change, which can either coincide with the direction of plastic changes (genetic assimilation) or be the opposite (genetic compensation). A special case of phenotypic plasticity is phenotypic change of the host caused by changes in its symbiotic microbiota. In the current review, we discuss the main forms of phenotypic plasticity and the current data on their impact on the rate and direction of evolutionary change. Special attention is paid to the results of recent experimental work, including the long-term evolutionary experiment on Drosophila melanogaster, which is being held at the Department of Evolutionary Biology, School of Biology, Moscow State University.

Maternal effect obscures adaptation to adverse environments and hinders divergence in Drosophila melanogaster

Adaptation to contrasting environments can facilitate ecological divergence and sympatric speciation. Factors that influence the probability and tempo of these processes are poorly known. We performed an evolutionary experiment on Drosophila melanogaster in order to attain better understanding of adaptation dynamics and to model the initial steps of sympatric speciation. In our experiment, several populations are being cultured either on standard rich medium (RM) or on nutrient-deficient starch-based medium (SM). After 10 generations, experimental populations demonstrated unexpected changes in their fitness: on the starch medium, flies grown on RM (FRM) outcompeted those that were cultured on SM (FSM), while on the rich medium, FRM were outcompeted by FSM. That is, experimental populations demonstrated higher fitness on the foreign medium, but were outcompeted by the aliens on the one they had been accustomed to. To explain the paradox, we hypothesize that the observed low fitness of FSM on SM was due to maternal effect, or the "effect of starving mother". The FSM flies are probably better adapted to SM, but the phenotypic outcome of their adaptations is obscured because the females grown on the poor medium invest less in their offspring (for instance, they may produce nutrient-deficient eggs). Larvae hatched from such eggs develop successfully on the rich medium RM, but experience delayed growth and/or lower survival rate on the nutrient-deficient medium SM. To test the hypothesis, we measured the fitness of the flies FSM after culturing them for one generation on RM, in order to remove the assumed maternal effect. As expected, this time FSM demonstrated higher fitness on SM compared to control flies (FRM) and to FSM before the removal of the maternal effect. The results support the idea that non-adaptive phenotypic plasticity and maternal effects can mask adaptation to adverse environments and prohibit ecological divergence and speciation by allowing the migrants from favourable habitats to outcompete resident individuals in adverse ecotopes despite the possible presence of specific adaptations in the latter.

Non-adaptive phenotypic plasticity: the effects of terrestrial and aquatic herbicides on larval salamander morphology and swim speed

Phenotypic plasticity, although ubiquitous, may not always be advantageous. Non-adaptive plasticity is likely to occur in response to novel environmental stress. Anthropogenic contaminants, such as herbicides, are novel stressors that are not present in the evolutionary history of most species. We investigated the pattern and consequences of phenotypic plasticity induced by four glyphosate-based herbicides (two terrestrial and two aquatic) in larvae of the spotted salamander, Ambystoma maculatum, by determining (1) whether the herbicides induced different morphologies; (2) if different morphologies translated to differences in burst swim performance; and (3) how induced individuals performed relative to non-induced controls. Different herbicide formulations led to the production of significantly different head and tail morphologies, and tail morphology correlated with fastest escape speed. However, escape speed did not vary among treatments. In addition, three out of four herbicide treatments experienced accelerated growth rates, in terms of the lateral size of tails, although the tail shapes were either similar to preliminary controls or intermediate between preliminary and final controls. These observations suggest that herbicide-induced morphology is a case of non-adaptive phenotypic plasticity, and that there is potentially a trade-off between growth and development for larvae exposed to different formulations. Understanding the functional significance of induced phenotypes is important for determining their importance in shaping an organism's ecological interactions and evolutionary trajectories. Furthermore, under different conditions, the morphological changes that we observed in response to exposure to herbicides might affect salamander fitness and influence population dynamics.

Non-adaptive phenotypic plasticity: the effects of terrestrial and aquatic herbicides on larval salamander morphology and swim speed

Non-adaptive phenotypic plasticity: the effects of terrestrial and aquatic herbicides on larval salamander morphology and swim speed

Ocean acidification and climate change: advances in ecology and evolution

Atmospheric CO2 concentration [CO2] has increased from a pre-industrial level of approximately 280 ppm to approximately 385 ppm, with further increases (700–1000 ppm) anticipated by the end of the twenty-first century [[1][1]]. Over the past three decades, changes in [CO2] have increased global

A critical appraisal of the predictive adaptive response hypothesis

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Adaptive Developmental Delay in Chagas Disease Vectors: An Evolutionary Ecology Approach

BackgroundThe developmental time of vector insects is important in population dynamics, evolutionary biology, epidemiology and in their responses to global climatic change. In the triatomines (Triatominae, Reduviidae), vectors of Chagas disease, evolutionary ecology concepts, which may allow for a better understanding of their biology, have not been applied. Despite delay in the molting in some individuals observed in triatomines, no effort was made to explain this variability.MethodologyWe applied four methods: (1) an e-mail survey sent to 30 researchers with experience in triatomines, (2) a statistical description of the developmental time of eleven triatomine species, (3) a relationship between development time pattern and climatic inter-annual variability, (4) a mathematical optimization model of evolution of developmental delay (diapause).Principal Findings85.6% of responses informed on prolonged developmental times in 5th instar nymphs, with 20 species identified with remarkable developmental delays. The developmental time analysis showed some degree of bi-modal pattern of the development time of the 5th instars in nine out of eleven species but no trend between development time pattern and climatic inter-annual variability was observed. Our optimization model predicts that the developmental delays could be due to an adaptive risk-spreading diapause strategy, only if survival throughout the diapause period and the probability of random occurrence of “bad” environmental conditions are sufficiently high.Conclusions/SignificanceDevelopmental delay may not be a simple non-adaptive phenotypic plasticity in development time, and could be a form of adaptive diapause associated to a physiological mechanism related to the postponement of the initiation of reproduction, as an adaptation to environmental stochasticity through a spreading of risk (bet-hedging) strategy. We identify a series of parameters that can be measured in the field and laboratory to test this hypothesis. The importance of these findings is discussed in terms of global climatic change and epidemiological consequences.

Evolutionary Biology of Animal Cognition

▪ Abstract This review focuses on five key evolutionary issues pertaining to animal cognition, defined as the neuronal processes concerned with the acquisition, retention, and use of information. Whereas the use of information, or decision making, has been relatively well examined by students of behavior, evolutionary aspects of other cognitive traits that affect behavior, including perception, learning, memory, and attention, are less well understood. First, there is ample evidence for genetically based individual variation in cognitive traits, although much of the information for some traits comes from humans. Second, several studies documented positive association between cognitive abilities and performance measures linked to fitness. Third, information on the evolution of cognitive traits is available primarily for color vision and decision making. Fourth, much of the data on plasticity of cognitive traits appears to reflect nonadaptive phenotypic plasticity, perhaps because few evolutionary analyses of cognitive plasticity have been carried out. Nonetheless, several studies suggest that cognitive traits show adaptive plasticity, and at least one study documented genetically based individual variation in plasticity. Fifth, whereas assertions that cognition has played a central role in animal evolution are not supported by currently available data, theoretical considerations indicate that cognition may either increase or decrease the rate of evolutionary change.

Is seasonal variation in leaf traits adaptive for the annual plant Dicerandra linearifolia?

Abstract Empirical studies of phenotypic plasticity have often relied on the plausibility that a plastic response to the environment would increase fitness in order to diagnose the response as adaptive. I conducted a test of the hypothesis that seasonal variation in leaf traits is an adaptive response to seasonal variation in environmental conditions faced by the annual plant Dicerandralinearifolia. This species exhibits variation in leaf morphology and anatomy in response to temperature that is consistent with the expectations for adaptive plasticity. I examined variation in the size, thickness and density of stomata of leaves that develop in summer and winter and used analysis of phenotypic selection during winter and summer seasons to test the hypothesis that seasonal variation in these traits is adaptive. Regression analyses of estimated dry mass (as a proxy for fitness) on leaf traits revealed no evidence supporting the adaptive hypothesis. Selection favoured individuals with large and thick leaves in both winter and summer, and density of stomata had little or no effect on estimated relative fitness in any season. Correspondence between seasonal variation in leaf thickness and density of stomata and expectations for adaptive plasticity appears to be purely fortuitous. Seasonal variation in leaf traits may persist simply because there is no selection against individuals in which these traits vary. My results underscore the importance of definitive tests of the hypothesis of adaptation to distinguish adaptive plasticity from neutral or nonadaptive phenotypic plasticity.

Rejection of non-adaptive hypotheses for intraspecific variation in trophic morphology in gape-limited predators

Recent studies have interpreted intraspecific divergence in relative head sizes in snakes as evidence for adaptation of the trophic apparatus in gape-limited predators to local prey size. However, such variation might also arise from non-adaptive processes (such as allometry, correlated response, genetic drift, or non-adaptive phenotypic plasticity). We test predictions from these alternative hypotheses using data on the allometric relationship between head size and body size in two wide-ranging snake species: eight populations of adders (Vipera berus) and 30 populations of common gartersnakes (Thamnophis sirtalis). Our data enable strong rejection of the alternative (non-adaptive) hypotheses, because the relationship between head and body size differed significantly among populations, the geographic distance separating pairs of populations explained less than 1.5% of their divergence in allometric coefficients, and the within-population allometric coefficients were higher than the among-population coefficients in each species. In addition, the geographical variability of allometric coefficients in females did not parallel that in males, suggesting that allometric coefficients have evolved independently in the two sexes. Phenotypic plasticity also cannot explain the data, because laboratory studies show that the allometric relationship between head size and body size is relatively insensitive to differing growth rates. We conclude that the intraspecific head size divergence in these snakes is better explained by spatially heterogeneous selection to optimize prey handling ability, than by non-adaptive processes.

Rejection of non-adaptive hypotheses for intraspecific variation in trophic morphology in gape-limited predators

Recent studies have interpreted intraspecific divergence in relative head sizes in snakes as evidence for adaptation of the trophic apparatus in gape-limited predators to local prey size. However, such variation might also arise from non-adaptive processes (such as allometry, correlated response, genetic drift, or non-adaptive phenotypic plasticity). We test predictions from these alternative hypotheses using data on the allometric relationship between head size and body size in two wide-ranging snake species: eight populations of adders (Vipera berus) and 30 populations of common gartersnakes (Thamnophis sirtalis). Our data enable strong rejection of the alternative (non-adaptive) hypotheses, because the relationship between head and body size differed significantly among populations, the geographic distance separating pairs of populations explained less than 1.5% of their divergence in allometric coefficients, and the within-population allometric coefficients were higher than the among-population coefficients in each species. In addition, the geographical variability of allometric coefficients in females did not parallel that in males, suggesting that allometric coefficients have evolved independently in the two sexes. Phenotypic plasticity also cannot explain the data, because laboratory studies show that the allometric relationship between head size and body size is relatively insensitive to differing growth rates. We conclude that the intraspecific head size divergence in these snakes is better explained by spatially heterogeneous selection to optimize prey handling ability, than by non-adaptive processes.