Genetic drift and rapid evolution of viviparity in insular fire salamanders (Salamandra salamandra)

Continental islands offer an excellent opportunity to investigate adaptive processes and to time microevolutionary changes that precede macroevolutionary events. We performed a population genetic study of the fire salamander (Salamandra salamandra), a species that displays unique intraspecific diversity of reproductive strategies, to address the microevolutionary processes leading to phenotypic and genetic differentiation of island, coastal and interior populations. We used eight microsatellite markers to estimate genetic diversity, population structure and demographic parameters in viviparous insular populations and ovoviviparous coastal and interior populations. Our results show considerable genetic differentiation (F(ST) range: 0.06-0.27), and no clear signs of gene flow among populations, except between the large and admixed interior populations. We find no support for island colonization by rafting or intentional/accidental anthropogenic introductions, indicating that rising sea levels were responsible for isolation of the island populations approximately 9000 years ago. Our study provides evidence of rapid genetic differentiation between island and coastal populations, and rapid evolution of viviparity driven by climatic selective pressures on island populations, geographic isolation with genetic drift, or a combination of these factors. Studies of these viviparous island populations in early stages of divergence help us better understand the microevolutionary processes involved in rapid phenotypic shifts.     

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.     

Predation- and competition-mediated brain plasticity in Rana temporaria tadpoles

An increasing number of studies have demonstrated phenotypic plasticity in brain size and architecture in response to environmental variation. However, our knowledge on how brain architecture is affected by commonplace ecological interactions is rudimentary. For example, while intraspecific competition and risk of predation are known to induce adaptive plastic modifications in morphology and behaviour in a wide variety of organisms, their effects on brain development have not been studied. We studied experimentally the influence of density and predation risk on brain development in common frog (Rana temporaria) tadpoles. Tadpoles grown at low density and under predation risk developed smaller brains than tadpoles at the other treatment combinations. Further, at high densities, tadpoles developed larger optic tecta and smaller medulla oblongata than those grown at low densities. These results demonstrate that ecological interactions - like intraspecific competition and predation risk - can have strong effects on brain development in lower vertebrates.     

Adaptive divergence vs. environmental plasticity: tracing local genetic adaptation of metamorphosis traits in salamanders

In order to assess the significance of local adaptation relative to environmental plasticity on the evolution of life history traits, we analysed the possible genetic basis of differences between pond- and stream-breeding fire salamanders (Salamandra salamandra) in Germany. These salamanders typically deposit their larvae in small streams, where they grow until they are sufficiently large to metamorphose. However, some populations in Western Germany use ponds as larval habitat. Because habitat quality of streams differs from that of ponds one expects life history differences in the pond animals, which may result either from a plastic response or through genetic differentiation (i.e. local adaptation). Using a phylogeographical analysis of mitochondrial D-loop sequences, we show that both stream and pond populations in Western Germany are derived from a single lineage that recolonized following the last glaciation. This finding suggests that pond breeding originated very recently. Our studies of habitat quality and metamorphic behaviour of larvae in natural ponds and streams disclosed that pond larvae experience a significantly reduced food supply and greater risk of drying than do stream larvae. Pond larvae metamorphose earlier at the cost of reduced mass. Common-environment experiments with pond and stream larvae show that metamorphic behaviour of pond larvae under limited-food conditions is determined genetically and is not simply a plastic response to the differing habitat conditions. These results show that phenotypic plasticity is less important than local adaptation in explaining differences in ecological diversification within this species and suggests the possibility of rapid evolution of genetic adaptations when new habitats are exploited.     

The alignment between phenotypic plasticity,the major axis of genetic variation and the response to selection

Phenotypic plasticity is the ability of a genotype to produce more than one phenotype in order to match the environment. Recent theory proposes that the major axis of genetic variation in a phenotypically plastic population can align with the direction of selection. Therefore, theory predicts that plasticity directly aids adaptation by increasing genetic variation in the direction favoured by selection and reflected in plasticity. We evaluated this theory in the freshwater crustacean Daphnia pulex, facing predation risk from two contrasting size-selective predators. We estimated plasticity in several life-history traits, the G matrix of these traits, the selection gradients on reproduction and survival, and the predicted responses to selection. Using these data, we tested whether the genetic lines of least resistance and the predicted response to selection aligned with plasticity. We found predator environment-specific G matrices, but shared genetic architecture across environments resulted in more constraint in the G matrix than in the plasticity of the traits, sometimes preventing alignment of the two. However, as the importance of survival selection increased, the difference between environments in their predicted response to selection increased and resulted in closer alignment between the plasticity and the predicted selection response. Therefore, plasticity may indeed aid adaptation to new environments.     

Environmental stress and the costs of whole-organism phenotypic plasticity in tadpoles

Costs of phenotypic plasticity are important for the evolution of plasticity because they prevent organisms from shaping themselves at will to match heterogeneous environments. These costs occur when plastic genotypes have relatively low fitness regardless of the trait value expressed. We report two experiments in which we measured selection on predator-induced plasticity in the behaviour and external morphology of frog tadpoles (Rana temporaria). We assessed costs under stressful and benign conditions, measured fitness as larval growth rate or competitive ability and focused analysis on aggregate measures of whole-organism plasticity. There was little convincing evidence for a cost of phenotypic plasticity in our experiments, and costs of canalization were nearly as frequent as costs of plasticity. Neither the magnitude of the cost nor the variation around the estimate (detectability) was sensitive to environmental stress.     

A comparative analysis of predator-induced plasticity in larval Triturus newts

Species that occupy similar habitats are expected to show convergent phenotypes. If habitats are defined by the presence of predators, then traits that modify vulnerability to predation, including predator-induced phenotypic plasticity, should be similar within habitats. We tested this idea using larvae of six syntopic newt species belonging to the two Triturus clades. Behavioural plasticity induced by odonate predators was strongly dissimilar between the two main clades but similar within them. Morphological plasticity was variable among species, even between one pair of closely related species. A predation experiment tested whether differences between clades could be caused by differences in body size. Size-specific vulnerability differed between newts in the small-bodied and large-bodied clades, indicating that similar predators may affect the two clades differently. The results showed both similarity and dissimilarity in predator-induced phenotypic plasticity in syntopic larval newts although theory suggests that divergence is unlikely in such ecologically similar species.     

Geographic variation and plasticity to water and nutrients in Pelargonium australe

Here, patterns of phenotypic plasticity and trait integration of leaf characteristics in six geographically discrete populations of the perennial herb Pelargonium australe were compared. It was hypothesized that populations would show local adaptation in trait means, but similar patterns of plasticity and trait integration. Further, it was questioned whether phenotypic plasticity was positively correlated with environmental heterogeneity and whether plasticity for water-use traits in particular was adaptive. Seedlings were grown in a glasshouse at six combinations of water and nutrient availability. Leaf anatomical, morphological and gas exchange traits were measured. High amounts of plasticity in leaf traits were found in response to changes in growth conditions and there was evidence of local adaptation among the populations. While there were significant correlations between plasticity and environmental heterogeneity, not all were positive. Notably, patterns of plasticity and trait integration varied significantly among populations. Despite that variation, some of the observed plasticity was adaptive: fitness was correlated with conservative water use when water was limiting. Pelargonium arrived in Australia approximately 5 million yr ago. It is concluded here that high amounts of plasticity, in some cases adaptive, and weak integration among traits may be key to the spread and success of this species.     

Testing limits to adaptation along altitudinal gradients in rainforest Drosophila

Given that evolution can generate rapid and dramatic shifts in the ecological tolerance of a species, what prevents populations adapting to expand into new habitat at the edge of their distributions? Recent population genetic models have focused on the relative costs and benefits of migration between populations. On the one hand, migration may limit adaptive divergence by preventing local populations from matching their local selective optima. On the other hand, migration may also contribute to the genetic variance necessary to allow populations to track these changing optima. Empirical evidence for these contrasting effects of gene flow in natural situations are lacking, largely because it remains difficult to acquire. Here, we develop a way to explore theoretical models by estimating genetic divergence in traits that confer stress resistance along similar ecological gradients in rainforest Drosophila. This approach allows testing for the coupling of clinal divergence with local density, and the effects of genetic variance and the rate of change of the optimum on the response to selection. In support of a swamping effect of migration on phenotypic divergence, our data show no evidence for a cline in stress-related traits where the altitudinal gradient is steep, but significant clinal divergence where it is shallow. However, where clinal divergence is detected, sites showing trait means closer to the presumed local optimum have more genetic variation than sites with trait means distant from their local optimum. This pattern suggests that gene flow also aids a sustained response to selection.     

Lack of local adaptation of invasive crofton weed (Ageratina adenophora) in different climatic areas of Yunnan Province,China

Aims Crofton weed, with a subtropical origin, has successfully invaded in diverse habitats that belong to different climate zones in Southwest China. We tested whether local adaptation plays an important role in the successful invasion of crofton weed in heterogeneous environments.Methods Five populations from different habitats with an altitude ranging from 678 to 2356 m were selected. Plant height, biomass, seed yield and seed germination capability of these populations were investigated in the field. Greenhouse and reciprocal transplant experiments with the five populations were conducted, and all the above characters were measured and compared among these populations.Important findings Plant height, biomass, seed yield and seed germination rate were each significantly different among the five populations in field. However, there was no difference among these populations in the greenhouse experiment. In the reciprocal transplant experiment, plants from the five populations responded similarly to different habitats in the field, indicating lack of local adaptation. Instead, phenotypic plasticity likely plays a key role in the invasion success of crofton weed in different habitats.     

Influence of learning on range expansion and adaptation to novel habitats

Learning has been postulated to ‘drive’ evolution, but its influence on adaptive evolution in heterogeneous environments has not been formally examined. We used a spatially explicit individual‐based model to study the effect of learning on the expansion and adaptation of a species to a novel habitat. Fitness was mediated by a behavioural trait (resource preference), which in turn was determined by both the genotype and learning. Our findings indicate that learning substantially increases the range of parameters under which the species expands and adapts to the novel habitat, particularly if the two habitats are separated by a sharp ecotone (rather than a gradient). However, for a broad range of parameters, learning reduces the degree of genetically‐based local adaptation following the expansion and facilitates maintenance of genetic variation within local populations. Thus, in heterogeneous environments learning may facilitate evolutionary range expansions and maintenance of the potential of local populations to respond to subsequent environmental changes.     

Variation in inbreeding depression and plasticity across native and non-native field environments

Background and Aims

Since the early 1990s, research on genetic variation of phenotypic plasticity has expanded and empirical research has emphasized the role of the environment on the expression of inbreeding depression. An emerging question is how these two evolutionary ecology mechanisms interact in novel environments. Interest in this area has grown with the need to understand the establishment of populations in response to climate change, and to human-assisted transport to novel environments.

Methods

We compare performance in the field of outcrossed (O) and inbred lines (S1, S2) from 20 maternal families from each of two native populations of Mimulus guttatus. The experiment was planted in California in each population''s home site, in the other populations''s home site, in a novel site within the native range of M. guttatus, and in a novel site within the non-native range in North America. The experiment included nearly 6500 individuals. Survival, sexual reproduction and above-ground biomass were examined in order to evaluate inbreeding depression, and stem diameter and plant height were examined in order to evaluate phenotypic plasticity.

Key Results

Across all field sites, approx. 36 % of plants survived to flowering. Inbreeding depression differed among sites and outcrossed offspring generally outperformed selfed offspring. However, in the native-novel site, self-progeny performed better or equally well as outcross progeny. Significant phenotypic plasticity and genetic variation in plasticity was detected in the two architectural traits measured. The absolute value of plasticity showed the most marked difference between home and non-native novel site or non-native-novel site. Evidence was detected for an interaction between inbreeding and plasticity for stem diameter.

Conclusions

The results demonstrate that during initial population establishment, both inbreeding depression and phenotypic plasticity vary among field sites, and may be an important response to environments outside a species'' currently occupied range. However, the interaction between inbreeding and plasticity may be limited and environment-dependent.     

Local adaptation in populations of a Brachionus group plicatilis cryptic species inhabiting three deep crater lakes in Central Mexico

1. Salinity is a strong selective force for many aquatic organisms, affecting both ecological and evolutionary processes. Most of our knowledge on the effects of salinity on rotifers in the Brachionus plicatilis species complex is based mainly on populations from waterbodies that experience broad environmental changes both seasonally and annually. We tested the hypothesis that, despite the supposedly high potential for gene flow among rotifers inhabiting neighbouring environments, constant salinity has promoted local adaptation, genetic population divergence and even cryptic speciation in B. plicatilis complex populations from three deep maar lakes of distinct salinities [1.1, 6.5 and 9.0 g L^?1 total dissolved solids (TDS)] in Central Mexico. 2. To look for local adaptation, we performed common garden experiments to test the effect of different salinities on population density and intrinsic growth rate (r). Then, we evaluated the genetic divergence by sequencing the cytochrome c oxidase subunit I (COI) gene and performed reproductive trials to assess the potential gene flow among the three populations and with other closely related B. plicatilis complex species. 3. We confirmed that the rotifer populations have phenotypic plasticity in tolerance of salinity, but only rotifers from the least saline lake are adapted to low salinity. Among the populations, sequence divergence at COI was very low (just a single haplotype was found), suggesting a persistent founder effect from a relatively recent single colonisation event and a subsequent dispersal from one lake to the others, and a very restricted immigration rate. In the phylogenetic analysis, rotifers from this area of Mexico clustered in the same clade with the middle‐sized species Brachionus ibericus and B. sp. ‘Almenara’. Mexican rotifers showed successful recognition, copulation and formation of hybrids among them, but interpopulation breeding with the Spanish B. ibericus and B. sp. ‘Almenara’ was unsuccessful. 4. We conclude that the B. plicatilis complex populations from these three lakes belong to a new biological species not yet described (presently named B. sp. ‘Mexico’). To our knowledge, this is the first report of local adaptation of a natural B. plicatilis complex population living in freshwater conditions (1.1 g L^?1 TDS).     

Breeding Habitat Selection of Salamandra salamandra (Linnaeus, 1758) in the Most Arid Zone of its European Distribution Range: Application to Conservation Management

The influence of environmental variables on the selection of a water body as breeding habitat by Salamandra salamandra was studied in an arid zone located in the southwestern part of its distribution range. From November 2002 to October 2003, 50 water bodies were monitored in the south east of the Iberian Peninsula. Environmental data were submitted to a stepwise logistic regression analysis at macrohabitat, water body typology and microhabitat scales in order to establish the main factors influencing the use of a given water body as breeding habitat by this species. A significant degree of dependence between the reproduction of Salamandra salamandra and environmental variables was observed at all of these levels. These results should be taken into account when populations of this species are subjected to management and/or recovery programmes in arid areas.     

Insulin signalling underlies both plasticity and divergence of a reproductive trait in Drosophila

Phenotypic plasticity is the ability of a single genotype to yield distinct phenotypes in different environments. The molecular mechanisms linking phenotypic plasticity to the evolution of heritable diversification, however, are largely unknown. Here, we show that insulin/insulin-like growth factor signalling (IIS) underlies both phenotypic plasticity and evolutionary diversification of ovariole number, a quantitative reproductive trait, in Drosophila. IIS activity levels and sensitivity have diverged between species, leading to both species-specific ovariole number and species-specific nutritional plasticity in ovariole number. Plastic range of ovariole number correlates with ecological niche, suggesting that the degree of nutritional plasticity may be an adaptive trait. This demonstrates that a plastic response conserved across animals can underlie the evolution of morphological diversity, underscoring the potential pervasiveness of plasticity as an evolutionary mechanism.     

Fine-scale thermal adaptation in a green turtle nesting population

The effect of climate warming on the reproductive success of ectothermic animals is currently a subject of major conservation concern. However, for many threatened species, we still know surprisingly little about the extent of naturally occurring adaptive variation in heat-tolerance. Here, we show that the thermal tolerances of green turtle (Chelonia mydas) embryos in a single, island-breeding population have diverged in response to the contrasting incubation temperatures of nesting beaches just a few kilometres apart. In natural nests and in a common-garden rearing experiment, the offspring of females nesting on a naturally hot (black sand) beach survived better and grew larger at hot incubation temperatures compared with the offspring of females nesting on a cooler (pale sand) beach nearby. These differences were owing to shallower thermal reaction norms in the hot beach population, rather than shifts in thermal optima, and could not be explained by egg-mediated maternal effects. Our results suggest that marine turtle nesting behaviour can drive adaptive differentiation at remarkably fine spatial scales, and have important implications for how we define conservation units for protection. In particular, previous studies may have underestimated the extent of adaptive structuring in marine turtle populations that may significantly affect their capacity to respond to environmental change.     

Phenotypic convergence along a gradient of predation risk

A long-standing question in ecology is whether phenotypic plasticity, rather than selection per se, is responsible for phenotypic variation among populations. Plasticity can increase or decrease variation, but most previous studies have been limited to single populations, single traits and a small number of environments assessed using univariate reaction norms. Here, examining two genetically distinct populations of Daphnia pulex with different predation histories, we quantified predator-induced plasticity among 11 traits along a fine-scale gradient of predation risk by a predator (Chaoborus) common to both populations. We test the hypothesis that plasticity can be responsible for convergence in phenotypes among different populations by experimentally characterizing multivariate reaction norms with phenotypic trajectory analysis (PTA). Univariate analyses showed that all genotypes increased age and size at maturity, and invested in defensive spikes (neckteeth), but failed to quantitatively describe whole-organism response. In contrast, PTA quantified and qualified the phenotypic strategy the organism mobilized against the selection pressure. We demonstrate, at the whole-organism level, that the two populations occupy different areas of phenotypic space in the absence of predation but converge in phenotypic space as predation threat increases.     

Assortative mating and the role of phenotypic plasticity in male competition: implications for gene flow among host-associated parasitoid populations

Local adaptation is promoted when habitat or mating preferences reduce gene flow between populations. However, gene flow is not only a function of dispersal but also of the success of migrants in their new habitat. In this study I investigated mating preference in conjunction with phenotypic plasticity using Aphidius parasitoids adapted to different host species. Males actively attempted to assortatively mate, but actual mating outcomes were strongly influenced by the relative size of the adult males. Results are discussed in the context of assortative mating in combination with the success of migrant males in mitigating gene flow between host-associated parasitoid populations.