Adaptive phenotypic plasticity in a clonal invader

Organisms featuring wide trait variability and occurring in a wide range of habitats, such as the ovoviviparous New Zealand freshwater snail Potamopyrgus antipodarum, are ideal models to study adaptation. Since the mid‐19th century, P. antipodarum, characterized by extremely variable shell morphology, has successfully invaded aquatic areas on four continents. Because these obligately and wholly asexual invasive populations harbor low genetic diversity compared to mixed sexual/asexual populations in the native range, we hypothesized that (1) this phenotypic variation in the invasive range might be adaptive with respect to colonization of novel habitats, and (2) that at least some of the variation might be caused by phenotypic plasticity. We surveyed 425 snails from 21 localities across northwest Europe to attempt to disentangle genetic and environmental effects on shell morphology. We analyzed brood size as proxy for fitness and shell geometric morphometrics, while controlling for genetic background. Our survey revealed 10 SNP genotypes nested into two mtDNA haplotypes and indicated that mainly lineage drove variation in shell shape but not size. Physicochemical parameters affected both shell shape and size and the interaction of these traits with brood size. In particular, stronger stream flow rates were associated with larger shells. Our measurements of brood size suggested that relatively larger slender snails with relatively large apertures were better adapted to strong flow than counterparts with broader shells and relatively small apertures. In conclusion, the apparent potential to modify shell morphology plays likely a key role in the invasive success of P. antipodarum; the two main components of shell morphology, namely shape and size, being differentially controlled, the former mainly genetically and the latter predominantly by phenotypic plasticity.     

Microsatellites: consensus and controversy

Microsatellite DNA loci have recently been adopted for many biological applications. Comparative studies across a wide range of species has revealed many details of their mutational properties and evolutionary life cycles. Experience shows that a full understanding of these processes is essential to ensure the effective use of microsatellites as analytical tools. In this article, we review the controversies that have arisen as biologists have taken up this new technology and the emerging consensus that has resulted from their debates. We point to the need for comparative DNA sequencing studies to produce input data for a new generation of theoretical models of microsatellite behaviour. We conclude by presenting our own conceptual model, ‘Snakes and Ladders’, as an aid to theory development.     

Adaptive phenotypic plasticity of gypsy moth digestive enzymes

The adaptiveness of plasticity of digestive enzyme responses to allelochemical stress was tested on 32 full-sib families of gypsy moth larvae from an oak forest population (the Quercus population) and 26 families from a locust-tree forest (the Robinia population), reared either on control diet, or on tannin-supplemented diet. Using the duration of larval development as an indirect measure of fitness, phenotypic selection analyses revealed that lower specific activities of total proteases and trypsin, and higher specific activity of leucine aminopeptidase were adaptive for both populations in the control environment. Plasticity was only shown to be costly for total proteases and trypsin activity in Quercus larvae. In a stressful environment, the most apparent adaptive response was a significant increase in lipase activity. There was no plasticity cost for lipase activity. The two populations differed in the direction of selection acting on α-glucosidase activity, which favoured decreased activity in Quercus larvae and increased activity in Robinia larvae in the control environment. α-glucosidase activity in Quercus larvae is characterized by cost of homeostasis, while cost of plasticity was shown for Robinia larvae. The results obtained on the plasticity of digestive enzyme activity indicate how this generalist species copes with variation in plant allelochemicals.     

Silk decorations: controversy and consensus

Although the occurrence of silk decorations has been noted in scientific literature for over 100 years, there is still little consensus as to their function. This is despite the proliferation of studies examining the five major hypotheses: (1) protection against predators, (2) increasing foraging success, (3) prevention of damage to the web, (4) providing shade and (5) mechanical support for the web. The first three of these hypotheses have received the most attention, and thus generated the most evidence (for and against) suggesting that web decorations are a type of visual signal. However, the effect of this signal on prey and predator receivers is unclear as the evidence is contradictory. Thus, the function of silk decorations may be context specific, depending on factors such as predators, prey, background colour and ambient light. A better understanding of how predators and prey see and process visual information from silk decorations, coupled with experiments examining the mechanisms behind the various hypotheses, are crucial in illuminating their function and resolving the controversy.     

Adaptive phenotypic plasticity: the case of heterophylly in aquatic plants

Phenotypic plasticity may play a key role in the adaptation of organisms to changing environmental conditions. A special case of plasticity is represented by heterophylly, the ability of semi-aquatic plants to produce different types of leaves below and above water. Submerged leaves are thin and lack both a cuticle and stomata, whereas aerial leaves are thicker, cutinized and bear stomata. The striking variability in the submerged, floating and aerial leaves of heterophyllous aquatics has historically been considered a paradigmatic example of adaptive phenotypic plasticity. An extensive body of developmental and physiological research reveals that heterophylly is quite often mediated by similar environmental cues across diverse taxa, which may imply a common underlying mechanism. Patterns of plasticity in response to environmental cues in the laboratory are consistent with the hypothesis of individual adaptation to heterogeneous environments, and the distribution of this trait among phylogenetically related aquatic angiosperms suggests either convergent or parallel evolution in their descent from terrestrial ancestors. Yet, critical evaluations of the ecological and evolutionary significance of this trait are scarce. In this essay, we discuss the patterns of plasticity revealed by experimental manipulative studies of heterophylly in the context of the general problem of adaptive phenotypic plasticity, and suggest avenues for future research that are needed in assessing the ecological and evolutionary significance of this trait.     

Adaptive phenotypic plasticity and the successful colonization of a novel environment

Behavior and other forms of phenotypic plasticity potentially enable individuals to deal with novel situations. This implies that establishment of a population in a new environment is aided by plastic responses, as first suggested by Baldwin (1896). In the early 1980s, a small population of dark-eyed juncos from a temperate, montane environment became established in a Mediterranean climate in coastal San Diego. The breeding season of coastal juncos is more than twice as long as that of the ancestral population, and they fledge approximately twice as many young. We investigated the adaptive significance of the longer breeding season and its consequences for population persistence. Within the coastal population, individuals with longer breeding seasons have higher offspring production and recruitment, with no measured detrimental effects such as higher mortality or lower reproductive success the following year. Population size has remained approximately constant during the 6 years of study (1998-2003). The increase in reproductive effort in the coastal population contributes substantially to the persistence of this population because there is no evidence of density-dependent recruitment, which would otherwise negate the effects of increased fledgling production. These results provide the first quantitative support of Baldwin's proposition that plasticity can be crucial for population persistence during the early stages of colonization.     

Adiponectin and energy homeostasis: consensus and controversy

Adiponectin regulates energy homeostasis through the modulation of glucose and fatty acid metabolism in peripheral tissues. However, its central effect on energy balance remains unclear and controversial. Despite the disparate data, recent advances in our understanding of the signal transduction mechanisms used by adiponectin in the periphery and in the hypothalamus suggest that intracellular cross-talk between adiponectin, leptin and insulin may occur at several levels. The present review will summarize recent reports describing the peripheral and central effects of adiponectin and discuss progress concerning its molecular mechanisms. We will also particularly focus on apparent controversies and related mechanisms associated with the central effects of adiponectin on energy homeostasis.     

Adaptive phenotypic plasticity and local adaptation for temperature tolerance in freshwater zooplankton

Many organisms have geographical distributions extending from the tropics to near polar regions or can experience up to 30°C temperature variation within the lifespan of an individual. Two forms of evolutionary adaptation to such wide ranges in ambient temperatures are frequently discussed: local adaptation and phenotypic plasticity. The freshwater planktonic crustacean Daphnia magna, whose range extends from South Africa to near arctic sites, shows strong phenotypic and genotypic variation in response to temperature. In this study, we use D. magna clones from 22 populations (one clone per population) ranging from latitude 0° (Kenya) to 66° North (White Sea) to explore the contributions of phenotypic plasticity and local adaptation to high temperature tolerance. Temperature tolerance was studied as knockout time (time until immobilization, T_imm) at 37°C in clones acclimatized to either 20°C or 28°C. Acclimatization to 28°C strongly increased T_imm, testifying to adaptive phenotypic plasticity. At the same time, T_imm significantly correlated with average high temperature at the clones’ sites of origin, suggesting local adaptation. As earlier studies have found that haemoglobin expression contributes to temperature tolerance, we also quantified haemoglobin concentration in experimental animals and found that both acclimatization temperature (AccT) and temperature at the site of origin are positively correlated with haemoglobin concentration. Furthermore, Daphnia from warmer climates upregulate haemoglobin much more strongly in response to AccT, suggesting local adaptation for plasticity in haemoglobin expression. Our results show that both local adaptation and phenotypic plasticity contribute to temperature tolerance, and elucidate a possible role of haemoglobin in mediating these effects that differs along a cold–warm gradient.     

Adaptive patterns of phenotypic plasticity in laboratory and field environments in Drosophila melanogaster

Identifying mechanisms of adaptation to variable environments is essential in developing a comprehensive understanding of evolutionary dynamics in natural populations. Phenotypic plasticity allows for phenotypic change in response to changes in the environment, and as such may play a major role in adaptation to environmental heterogeneity. Here, the plasticity of stress response in Drosophila melanogaster originating from two distinct geographic regions and ecological habitats was examined. Adults were given a short‐term, 5‐day exposure to combinations of temperature and photoperiod to elicit a plastic response for three fundamental aspects of stress tolerance that vary adaptively with geography. This was replicated both in the laboratory and in outdoor enclosures in the field. In the laboratory, geographic origin was the primary determinant of the stress response. Temperature and the interaction between temperature and photoperiod also significantly affected stress resistance. In the outdoor enclosures, plasticity was distinct among traits and between geographic regions. These results demonstrate that short‐term exposure of adults to ecologically relevant environmental cues results in predictable effects on multiple aspects of fitness. These patterns of plasticity vary among traits and are highly distinct between the two examined geographic regions, consistent with patterns of local adaptation to climate and associated environmental parameters.     

Adaptive phenotypic plasticity and genetics of larval life histories in two Rana temporaria populations

Phenotypic plasticity provides means for adapting to environmental unpredictability. In terms of accelerated development in the face of pond-drying risk, phenotypic plasticity has been demonstrated in many amphibian species, but two issues of evolutionary interest remain unexplored. First, the heritable basis of plastic responses is poorly established. Second, it is not known whether interpopulational differences in capacity to respond to pond-drying risk exist, although such differences, when matched with differences in desiccation risk would provide strong evidence for local adaptation. We investigated sources of within- and among-population variation in plastic responses to simulated pond-drying risk (three desiccation treatments) in two Rana temporaria populations originating from contrasting environments: (1) high desiccation risk with weak seasonal time constraint (southern population); and (2) low desiccation risk with severe seasonal time constraint (northern population). The larvae originating from the environment with high desiccation risk responded adaptively to the fast decreasing water treatment by accelerating their development and metamorphosing earlier, but this was not the case in the larvae originating from the environment with low desiccation risk. In both populations, metamorphic size was smaller in the high-desiccation-risk treatment, but the effect was larger in the southern population. Significant additive genetic variation in development rate was found in the northern and was nearly significant in the southern population, but there was no evidence for genetic variation in plasticity for development rates in either of the populations. No genetic variation for plasticity was found either in size at metamorphosis or growth rate. All metamorphic traits were heritable, and additive genetic variances were generally somewhat higher in the southern population, although significantly so in only one trait. Dominance variances were also significant in three of four traits, but the populations did not differ. Maternal effects in metamorphic traits were generally weak in both populations. Within-environment phenotypic correlations between larval period and metamorphic size were positive and genetic correlations negative in both populations. These results suggest that adaptive phenotypic plasticity is not a species-specific fixed trait, but evolution of interpopulational differences in plastic responses are possible, although heritability of plasticity appears to be low. The lack of adaptive response to desiccation risk in northern larvae is consistent with the interpretation that selection imposed by shorter growing season has favored rapid development in north (approximately 8% faster development in north as compared to south) or a minimum metamorphic size at the expense of phenotypic plasticity.     

Adaptive developmental plasticity: Compartmentalized responses to environmental cues and to corresponding internal signals provide phenotypic flexibility

Background

The environmental regulation of development can result in the production of distinct phenotypes from the same genotype and provide the means for organisms to cope with environmental heterogeneity. The effect of the environment on developmental outcomes is typically mediated by hormonal signals which convey information about external cues to the developing tissues. While such plasticity is a wide-spread property of development, not all developing tissues are equally plastic. To understand how organisms integrate environmental input into coherent adult phenotypes, we must know how different body parts respond, independently or in concert, to external cues and to the corresponding internal signals.

Results

We quantified the effect of temperature and ecdysone hormone manipulations on post-growth tissue patterning in an experimental model of adaptive developmental plasticity, the butterfly Bicyclus anynana. Following a suite of traits evolving by natural or sexual selection, we found that different groups of cells within the same tissue have sensitivities and patterns of response that are surprisingly distinct for the external environmental cue and for the internal hormonal signal. All but those wing traits presumably involved in mate choice responded to developmental temperature and, of those, all but the wing traits not exposed to predators responded to hormone manipulations. On the other hand, while patterns of significant response to temperature contrasted traits on autonomously-developing wings, significant response to hormone manipulations contrasted neighboring groups of cells with distinct color fates. We also showed that the spatial compartmentalization of these responses cannot be explained by the spatial or temporal compartmentalization of the hormone receptor protein.

Conclusions

Our results unravel the integration of different aspects of the adult phenotype into developmental and functional units which both reflect and impact evolutionary change. Importantly, our findings underscore the complexity of the interactions between environment and physiology in shaping the development of different body parts.

     

Costs of phenotypic plasticity

Phenotypically plastic organisms display alternative phenotypes in different environments. It is widely appreciated that possessing alternative phenotypes can affect fitness. However, some investigators have suggested that simply carrying the ability to be plastic could also affect fitness. Evolutionary models suggest that high costs of plasticity could constrain the evolution of optimal phenotypes. However, costs (and limits) of plasticity are primarily hypothetical. Little empirical evidence exists to show that increased plasticity leads to reduced growth and development, leads to increased developmental instability, or limits the ability of organisms to produce more extreme phenotypes. I used half-sib families of larval wood frogs (Rana sylvatica) reared in outdoor mesocosms to examine how tadpoles altered behavioral, morphological, and life-historical traits in response to larval dragonfly predators (Anax longipes). The predators induced lower activity and the development of relatively large tails and small bodies in wood frogs. As a result, wood frogs experienced reduced growth and development. I then examined whether tadpole sibships with higher plasticity experienced fitness costs (above and beyond the costs of expressing a particular phenotype) and whether they were limited in producing extreme phenotypes. Fitness effects of plasticity were widespread. Depending on the trait examined and the environment experienced, increased plasticity had either positive effects, negative effects, or no effects on tadpole mass, development, and survivorship. I found no relationship between increased plasticity and greater developmental instability. There was also no evidence that sibships with increased plasticity produced less extreme phenotypes; the most extreme trait states were always produced by the most plastic genotypes. This work suggests that costs of plasticity may be pervasive in nature and may substantially impact the evolution of optimal phenotypes in organisms that live in heterogeneous environments.     

Repeat expansion and autosomal dominant neurodegenerative disorders: consensus and controversy

Repeat-expansion mutations cause 13 autosomal dominant neurodegenerative disorders falling into three groups. Huntington's disease (HD), dentatorubral pallidoluysian atrophy (DRPLA), spinal and bulbar muscular atrophy (SBMA), and spinocerebellar ataxias (SCAs) types 1, 2, 3, 7 and 17 are each caused by a CAG repeat expansion that encodes polyglutamine. Convergent lines of evidence demonstrate that neurodegeneration in these diseases is a consequence of the neurotoxic effects of abnormally long stretches of glutamines. How polyglutamine induces neurodegeneration, and why neurodegeneration occurs in only select neuronal populations, remains a matter of intense investigation. SCA6 is caused by a CAG repeat expansion in CACNA1A, a gene that encodes a subunit of the P/Q-type calcium channel. The threshold length at which the repeat causes disease is much shorter than in the other polyglutamine diseases, and neurodegeneration may arise from expansion-induced change of function in the calcium channel. Huntington's disease-like 2 (HDL2) and SCAs 8, 10 and 12 are rare disorders in which the repeats (CAG, CTG or ATTCT) are not in protein-coding regions. Investigation into these diseases is still at an early stage, but it is now reasonable to hypothesise that the net effect of each expansion is to alter gene expression. The different pathogenic mechanisms in these three groups of diseases have important implications for the development of rational therapeutics.     

Evolution of phenotypic plasticity: patterns of plasticity and the emergence of ecotypes

Phenotypic plasticity itself evolves, as does any other quantitative trait. A very different question is whether phenotypic plasticity causes evolution or is a major evolutionary mechanism. Existing models of the evolution of phenotypic plasticity cover many of the proposals in the literature about the role of phenotypic plasticity in evolution. I will extend existing models to cover adaptation to a novel environment, the appearance of ecotypes and possible covariation between phenotypic plasticity and mean trait value of ecotypes. Genetic assimilation does not sufficiently explain details of observed patterns. Phenotypic plasticity as a major mechanism for evolution--such as, invading new niches, speciation or macroevolution--has, at present, neither empirical nor model support.