Differentiation of movement behaviour in an adaptively diverging salamander population

Dispersal is considered to be a species‐specific trait, but intraspecific variation can be high. However, when and how this complex trait starts to differentiate during the divergence of species/lineages is unknown. Here, we studied the differentiation of movement behaviour in a large salamander population (Salamandra salamandra), in which individual adaptations to different habitat conditions drive the genetic divergence of this population into two subpopulations. In this system, salamanders have adapted to the deposition and development of their larvae in ephemeral ponds vs. small first‐order streams. In general, the pond habitat is characterized as a spatially and temporally highly unpredictable habitat, while streams provide more stable and predictable conditions for the development of larvae. We analysed the fine‐scale genetic distribution of larvae, and explored whether the adaptation to different larval habitat conditions has in turn also affected dispersal strategies and home range size of adult salamanders. Based on the genetic assignment of adult individuals to their respective larval habitat type, we show that pond‐adapted salamanders occupied larger home ranges, displayed long‐distance dispersal and had a higher variability of movement types than the stream‐adapted individuals. We argue that the differentiation of phenotypically plastic traits such as dispersal and movement characteristics can be a crucial component in the course of adaptation to new habitat conditions, thereby promoting the genetic divergence of populations.     

Smells like home: Desert ants, Cataglyphis fortis, use olfactory landmarks to pinpoint the nest

Background

Although some mechanisms of habitat adaptation of conspecific populations have been recently elucidated, the evolution of female preference has rarely been addressed as a force driving habitat adaptation in natural settings. Habitat adaptation of fire salamanders (Salamandra salamandra), as found in Middle Europe (Germany), can be framed in an explicit phylogeographic framework that allows for the evolution of habitat adaptation between distinct populations to be traced. Typically, females of S. salamandra only deposit their larvae in small permanent streams. However, some populations of the western post-glacial recolonization lineage use small temporary ponds as larval habitats. Pond larvae display several habitat-specific adaptations that are absent in stream-adapted larvae. We conducted mate preference tests with females from three distinct German populations in order to determine the influence of habitat adaptation versus neutral genetic distance on female mate choice. Two populations that we tested belong to the western post-glacial recolonization group, but are adapted to either stream or pond habitats. The third population is adapted to streams but represents the eastern recolonization lineage.

Results

Despite large genetic distances with F_ST values around 0.5, the stream-adapted females preferred males from the same habitat type regardless of genetic distance. Conversely, pond-adapted females did not prefer males from their own population when compared to stream-adapted individuals of either lineage.

Conclusion

A comparative analysis of our data showed that habitat adaptation rather than neutral genetic distance correlates with female preference in these salamanders, and that habitat-dependent female preference of a specific pond-reproducing population may have been lost during adaptation to the novel environmental conditions of ponds.     

Linking the evolution of habitat choice to ecosystem functioning: direct and indirect effects of pond-reproducing fire salamanders on aquatic-terrestrial subsidies

Shifts in life history traits and in the behaviour of species can potentially alter ecosystem functioning. The reproduction of the central European fire salamander (Salamandra salamandra), which usually deposits its larvae in first-order streams, in small pool and pond-like habitats, is an example of a recent local adaptation in this species. Here we aimed to quantify the direct and indirect effects of the predatory larvae on the aquatic food webs in the ponds and on the flux of matter between the ponds and adjacent terrestrial habitats. Our estimates are based on biomass data of the present pond fauna as well as on the analysis of stomach content data, growth rates and population dynamics of the salamander larvae in pond habitats. By their deposition of larvae in early spring, female fire salamanders import between 0.07 and 2.86 g dry mass m^?2 larval biomass into the ponds. Due to high mortality rates in the larval phase and the relatively small size at metamorphosis of the pond-adapted salamanders compared to stream-adapted ones, the biomass export of the metamorphosed salamanders clearly falls below the initial biomass import. Catastrophic events such as high water temperatures and low oxygen levels may even occasionally result in mass mortalities of salamander larvae and thus in a net 100 % import of the salamander biomass into the pond food webs. Indirect effects further accelerate this net import of matter into the aquatic habitat, e.g. the feeding of salamanders on aquatic insect larvae with the emergence of terrestrial adults—thus preventing export—and on terrestrial organisms that fall on the water surface (supporting import). This study demonstrates that the adaptation of salamanders to pond reproduction can alter food web linkages across ecosystem boundaries by enhancing the flux of materials and energy from terrestrial (i.e. forest) to the aquatic (i.e. pond) habitat.     

HABITAT DURATION,LENGTH OF LARVAL PERIOD,AND THE EVOLUTION OF A COMPLEX LIFE CYCLE OF A SALAMANDER,AMBYSTOMA TEXANUM

In many organisms, genotypic selection may be a less effective means of adapting to unpredictable environments than is selection for phenotypic plasticity. To determine whether genotypic selection is important in the evolution of complex life cycles of amphibians that breed in seasonally ephemeral habitats, we examined whether mortality risk from habitat drying in natural populations of small-mouthed salamanders (Ambystoma texanum) corresponded to length of larval period when larvae from the same populations were grown in a common laboratory environment. Comparisons were made at two levels of organization within the species: 1) among geographic races that are under strongly divergent selection regimes associated with the use of pond and stream habitats and 2) among populations within races that use the same types of breeding habitats. Morphological evidence indicates that stream-breeding A. texanum evolved from pond-breeding populations that recently colonized streams. Larvae in streams incur heavy mortality from stream drying, so the upper bound on length of larval period is currently set by the seasonal duration of breeding sites. We hypothesized that selection would reduce length of larval period of pond-breeders that colonize streams if their larval periods are inherently longer than those of stream-breeders. The results of laboratory experiments support this hypothesis. When grown individually in a common environment, larvae from stream populations had significantly shorter larval periods than larvae from pond populations. Within races, however, length of larval period did not correlate significantly with seasonal duration of breeding sites. When males of both races were crossed to a single pond female, offspring of stream males had significantly shorter larval periods than offspring of pond males. Collectively, these data suggest that differences in complex life cycles among pond and stream-breeders are due to genotypic selection related to mortality from habitat drying. Stream larvae in the common-environment experiment were significantly smaller at metamorphosis than pond larvae. Yet, the evolution of metamorphic size cannot be explained readily by direct selection: there are no intuitively obvious advantages of being relatively small at metamorphosis in streams. A positive phenotypic correlation was observed between size at metamorphosis and length of larval period in most laboratory populations. A positive additive genetic correlation between these traits was demonstrated recently in another amphibian. Thus, we suspect that metamorphic size of stream-breeders evolved indirectly as a consequence of selection to shorten length of larval period.     

There is no place like home: Larval habitat type and size affect risk-taking behaviour in fire salamander larvae (Salamandra salamandra)

Individual life histories are strongly influenced by early environmental conditions and experiences. They shape morphology as well as behaviour and can promote adaptive divergence and phenotypic plasticity with regard to different habitat types. The fire salamander (Salamandra salamandra) in the Kottenforst forest in Bonn, Germany, exhibits two genetically distinct ecotypes occurring in two larval habitats, either ponds or streams. In this study, we investigated whether both ecotypes differ in risk-taking behaviour, measured as the behavioural response during a shelter-emergence test and a shelter-seeking test, and whether larval habitat type and size impact these behaviours. Our results revealed an influence of size as well as habitat type. Larger larvae of both habitats appear to be more risk-prone, as they spent more time outside the starting shelter in the shelter-emergence test. Irrespective of size, pond larvae sought shelter more often in the shelter-seeking test and are thus considered to be less risk-prone. These results indicate that larvae conform to a given niche by adjusting their behaviour. Future studies are needed to disentangle the role of genetic adaptation or phenotypic plasticity and to investigate long-term consequences of the larval habitat for the adult phenotype. Thereby, efforts should be made to create a concise set of multiple tests assessing behavioural patterns.     

Correlated evolution of phenotypic plasticity in metamorphic timing

Phenotypic plasticity has long been a focus of research, but the mechanisms of its evolution remain controversial. Many amphibian species exhibit a similar plastic response in metamorphic timing in response to multiple environmental factors; therefore, more than one environmental factor has likely influenced the evolution of plasticity. However, it is unclear whether the plastic responses to different factors have evolved independently. In this study, we examined the relationship between the plastic responses to two experimental factors (water level and food type) in larvae of the salamander Hynobius retardatus, using a cause-specific Cox proportional hazards model on the time to completion of metamorphosis. Larvae from ephemeral ponds metamorphosed earlier than those from permanent ponds when kept at a low water level or fed conspecific larvae instead of larval Chironomidae. This acceleration of metamorphosis depended only on the permanency of the larvae's pond of origin, but not on the conspecific larval density (an indicator of the frequency of cannibalism) in the ponds. The two plastic responses were significantly correlated, indicating that they may evolve correlatively. Once plasticity evolved as an adaptation to habitat desiccation, it might have relatively easily become a response to other ecological factors, such as food type via the pre-existing developmental pathway.     

Sticklebacks from streams are more bold than sticklebacks from ponds

Risk-taking behaviour has important consequences for fitness. Here, we show that risk-taking behaviour in sticklebacks consistently varies according to the habitat of origin. We compared the risk-taking behaviour of individual sticklebacks from three pond and three stream populations. Specifically, we measured willingness to forage under predation risk following a simulated attack by a model heron predator. Sticklebacks from stream populations were more willing to forage under predation risk than fish from pond populations. Sticklebacks from streams resumed eating after the simulated attack faster and spent more time eating compared to sticklebacks from ponds. We discuss these findings in terms of differences in life history and predation pressure in the two habitat types.     

ADAPTIVE COLORATION AND GENE FLOW AS A CONSTRAINT TO LOCAL ADAPTATION IN THE STREAMSIDE SALAMANDER,AMBYSTOMA BARBOURI

Predation is an important selective force that influences animal color patterns. Some larval populations of the streamside salamander, Ambystoma barbouri, inhabit streams with fish predators. Other larval salamanders are found in shallow, ephemeral streams that are predator-free. Quantitative melanophore cell counts and estimates of percent body area pigmented indicated that larval coloration is strongly correlated with stream type. Larvae that coexist with fish tend to be lighter than larvae from streams that are Ashless and ephemeral. Two approaches demonstrated that lightly pigmented salamander larvae better match the common background in relatively permanent streams and are less conspicuous to fish than dark larvae. First, using a model based on the spectral sensitivity of the fish and reflectance properties of salamanders and natural stream backgrounds, we showed that light larvae are three times more cryptic than dark larvae on rocks. Second, lighter larvae had higher survival than darker salamanders on rocks in a predator- choice experiment. It is not clear why larvae in ephemeral streams are darker. Larvae in ephemeral streams should be active to feed and develop rapidly and reach sufficient size to metamorphose before seasonal drying. Several hypotheses may explain why larvae tend to be darker in ephemeral streams, such as increased thermoregulatory ability, better screening of ultraviolet radiation (in these shallower streams), or better background matching to terrestrial predators. Among populations where salamander larvae coexist with fish, there are differences in relative crypsis. Larvae from populations with fish and relatively high gene flow from ephemeral populations (where larvae are dark) tend to be darker (with more melanophores) and more conspicuous to predators than those from more genetically isolated populations, where larvae are lighter and more cryptic. These differences illustrate the role of gene flow as a constraint to adaptive evolution.     

PAEDOMORPHOSIS IN AMBYSTOMA TALPOIDEUM: MAINTENANCE OF POPULATION VARIATION AND ALTERNATIVE LIFE-HISTORY PATHWAYS

A “common garden” experiment using artifical ponds was performed to test if differences in frequency of paedomorphosis and metamorphosis among six natural populations of the salamander Ambystoma talpoideum resulted from the drying regime of the aquatic habitat acting as an agent of selection. Our experiment supports the hypothesis of genetic differentiation in the propensity to metamorphose among the populations, but gave mixed evidence that pond-drying regime is the selective force directing evolution of this trait. Some populations appear to have evolved phenotypic plasticity whereas others may have a genetic polymorphism in their propensity to metamorphose as ponds dry.     

Foraging tactics in alternative heterochronic salamander morphs: trophic quality of ponds matters more than water permanency

1. In lentic freshwater habitats, the composition of animal assemblages shifts along a gradient from temporary to permanent basins. When habitats with different degrees of permanence are at the scale of the home range of species, they constitute alternatives in terms of energy acquisition through feeding. 2. In this context, previous studies showed an advantage of metamorphic over paedomorphic tiger salamanders (Ambystoma tigrinum) in temporary ponds which are only available to metamorphs. The aim of this study was to establish whether salamanders obtain similar benefits in ponds that do not differ in water permanence and whether salamanders shifted from detrimental to advantageous ponds. To this end, we determined the feeding habits, body condition and movement patterns of the two morphs in a complex of four permanent and four temporary ponds. 3. Consistent with previous studies, metamorphs consumed higher‐quality diets than paedomorphs in term of energy intake. However, these differences occurred because metamorphs consumed fairy shrimp in a single temporary pond. Individual movement patterns confirmed that most of the metamorphs used different aquatic habitats both within and between years and that most of them moved from permanent ponds for breeding towards the most profitable temporary pond in terms of foraging. 4. These results indicate that habitat selection by salamanders is optimal in term of energy intake in metamorphs that use high quality ponds independently of hydroperiod. It seems that both spatial and temporal variation can influence the relative foraging success of each morph.     

Reaction norms for metamorphic traits in natterjack toads to larval density and pond duration

The evolution of environmentally-induced changes in phenotype or reaction norm implies both the existence at some time of genetic variation within a population for that plasticity measured by the presence of genotype x environment interaction (G x E), and that phenotypic variation affects fitness. Otherwise, the genetic structure of polygenic traits may restrict the evolution of the reaction norm by the lack of independent evolution of a given trait in different environments or by genetic trade-offs with other traits that affect fitness. In this paper, we analyze the existence of G x E in metamorphic traits to two environmental factors, larval density and pond duration in a factorial experiment with Bufo calamita tadpoles in semi-natural conditions and in the laboratory. Results showed no plastic temporal response in metamorphosis to pond durability at low larval density. The rank of genotypes did not change across different hydroperiods, implying a high genetic correlation that may constrain the evolution of the reaction norm. At high larval density a significant G x E interaction was found, suggesting the potential for the evolution of the reaction norm. A sibship (#1) attained the presumed “optimal” reaction norm by accelerating developmental rate in short duration ponds and delaying it in longer ponds. This could be translated in fitness by an increment in metamorphic survival and size at metamorphosis in short and long ponds respectively with respect to non-plastic sibships. However, genetic variability for plasticity suggests that optimal reaction norm for developmental rates may be variable and hard to achieve in the heterogeneous pond environment. Mass at metamorphosis was not plastic across different pond durations but decreased at high larval density. Significant adaptive plasticity for growth rates appeared in environments that differed drastically in level of crowding conditions, both in the field and in the laboratory. The fact that survival of juveniles metamorphosed at high density ponds was a monotonic function of metamorphic size, implies that response to selection may occur in this population of natterjacks and that genetic variability in plasticity may be a reliable mechanism maintaining adaptive genetic variation in growth rates in the highly variable pond environment.     

Distribution, abundance, and genetic diversity of Clinostomum spp. metacercariae (Trematoda:Digenea) in a modified Ozark stream system

Land-use alterations can have profound influences on faunal distributions, including host-parasite relationships. Yellow grub trematodes ( Clinostomum spp.) have complex life cycles involving 3 hosts: a snail, a fish or amphibian, and a bird. Here, we analyze the distribution, prevalence, intensity, abundance, and genetic diversity of encysting metacercariae of Clinostomum spp. in salamanders and fishes throughout an aquatic system that includes a natural Ozark stream and man-made ponds. We found Clinostomum sp. infecting permanently aquatic Oklahoma salamanders ( Eurycea tynerensis ; 56% prevalence) and larval grotto salamanders ( Eurycea spelaea ) immediately downstream from a man-made pond. However, Clinostomum sp. did not infect any salamanders in the spring that supplies this pond, or in sections farther downstream (~0.5 and 2 km). Metacercariae of Clinostomum sp. were present in ~90% of introduced largemouth bass ( Micropterus salmoides ) in the man-made pond adjunct to the stream. Morphological examination and phylogenetic analyses based on the mitochondrial gene cytochrome oxidase 1 ( Co1 ) and the nuclear ribosomal gene 18S show that fishes and salamanders at this site are primarily infected with Clinostomum marginatum . There is a relatively high degree of mitochondrial haplotype diversity in C. marginatum at this site but no consistent genetic difference between parasites in largemouth bass from the man-made pond and those in salamanders from the stream. Based on the microgeographic distribution and relationships of metacercariae of C. marginatum at this site, we hypothesize that the adjunct man-made pond has created an ecological situation that brings the cercariae of this parasite into contact with novel stream salamander hosts.     

Variation in the degree and costs of adaptive phenotypic plasticity among Rana temporaria populations

Adaptive phenotypic plasticity in the form of capacity to accelerate development as a response to pond drying risk is known from many amphibian species. However, very little is known about factors that might constrain the evolution of this type of plasticity, and few studies have explored to what degree plasticity might be constrained by trade-offs dictated by adaptation to different environmental conditions. We compared the ability of southern and northern Scandinavian common frog (Rana temporaria) larvae originating from 10 different populations to accelerate their development in response to simulated pond drying risk and the resulting costs in metamorphic size in a factorial laboratory experiment. We found that (i) northern larvae developed faster than the southern larvae in all treatments, (ii) a capacity to accelerate the response was present in all five southern and all five northern populations tested, but that the magnitude of the response was much larger (and less variable) in the southern than in the northern populations, and that (iii) significant plasticity costs in metamorphic size were present in the southern populations, the plastic genotypes having smaller metamorphic size in the absence of desiccation risk, but no evidence for plasticity costs was found in the northern populations. We suggest that the weaker response to pond drying risk in the northern populations is due to stronger selection on large metamorphic size as compared with southern populations. In other words, seasonal time constraints that have selected the northern larvae to be fast growing and developing, may also constrain their innate ability for adaptive phenotypic plasticity.     

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.     

Habitat fragmentation as a result of biotic and abiotic factors controls pathogen transmission throughout a host population

1. The hypothesis that habitat fragmentation (biotic or abiotic) alters the transmission of disease within a population is explored using field data from a well-studied amphibian-pathogen system. 2. We used the Ambystoma tigrinum-A. tigrinum virus (ATV) model system to show how habitat fragmentation as a result of emergent vegetation and habitat management affects disease transmission dynamics in ponds across a landscape. 3. We quantified variation in ATV infection over time and across the landscape. ATV infection was significantly higher in ponds modified for livestock use (P = 0.032). Disease incidence decreased with increased amounts of emergent vegetation (P < 0.001). These factors appear to control disease transmission by altering the host contact rate and with it disease transmission. 4. A field experiment to test the effect of emergent vegetation on the distribution of larvae in ponds demonstrated a behavioural change in larvae found in sparsely vegetated ponds. Microhabitat choices resulted in larvae being concentrated at the pond edge resulting in a 'halo effect' in sparsely vegetated ponds, whereas larvae in heavily vegetated ponds were distributed more evenly throughout. Microhabitat choice affects the effective density that larvae experience. This 'halo effect' increases contact rates in the shallows of sparsely vegetated ponds and increases the transmission of a directly transmitted pathogen. 5. Despite recurrent epidemics of a lethal Ranavirus in tiger salamanders on the Kaibab Plateau, Arizona, USA, these populations persist. We discuss the implications of our results in the context of density-dependent transmission and homogeneous mixing, two increases key assumptions of epidemiological theory.     

Habitat specialization and adaptive phenotypic divergence of anuran populations

We tested for adaptive population structure in the frog Rana temporaria by rearing tadpoles from 23 populations in a common garden experiment, with and without larval dragonfly predators. The goal was to compare tadpole phenotypes with the habitats of their source ponds. The choice of traits and habitat variables was guided by prior information about phenotypic function. There were large differences among populations in life history, behaviour, morphological shape, and the predator-induced plasticities in most of these. Body size and behaviour were correlated with predation risk in the source pond, in agreement with adaptive population divergence. Tadpoles from large sunny ponds were morphologically distinct from those inhabiting small woodland ponds, although here an adaptive explanation was unclear. There was no evidence that plasticity evolves in populations exposed to more variable environments. Much among-population variation in phenotype and plasticity was not associated with habitat, perhaps reflecting rapid changes in wetland habitats.     

Spatiotemporal allozyme variation in the damselfly, <Emphasis Type="BoldItalic">Lestes viridis</Emphasis> (Odonata: Zygoptera): gene flow among permanent and temporary ponds

Several insect species seem to persist not only in permanent but also in temporary ponds where they face particularly harsh conditions and frequent extinctions. Under such conditions, gene flow may prevent local adaptation to temporary ponds and may promote phenotypic plasticity, or maintain apparent population persistence. The few empirical studies on insects suggest the latter mechanism, but no studies so far quantified gene flow including both pond types. We investigated the effects of pond type and temporal variation on population genetic differentiation and gene flow in the damselfly Lestes viridis in northern Belgium. We report a survey of two allozyme loci (Gpi, Pgm) with polyacrylamide gel electrophoresis in 14 populations from permanent and temporary ponds, and compared these results with similar data from the same permanent populations one year before. The data suggested that neither pond-drying regime, nor temporal variation have a substantial effect on population genetic structuring and did not provide evidence for stable population differentiation in L. viridis in northern Belgium. Gene flow estimates were high within permanent and temporary ponds, and between pond types. Our data are consistent with a source-sink metapopulation system where temporary ponds act as sinks in dry years, and are quickly recolonized after local population extinction. This may create a pattern of apparent population persistence of this species in permanent and temporary ponds without clear local adaptation.     

Fish assemblages in temporary ponds adjacent to 'terra-firme' streams in Central Amazonia

1. The effect of habitat structural features and physicochemical characteristics of the water on the composition and richness of fish assemblages in temporary ponds near streams were examined at three spatial scales: among ponds, among streams and between drainage basins, in a ‘terra‐firme’ (not subject to long‐term flooding) forest reserve in Central Amazonia. 2. The fish assemblage in temporary ponds was composed of subsets of 18 small‐bodied species widely distributed in the reserve. The assemblages had a nested subset structure, where smaller ponds contained subgroups of the species found in larger ponds. 3. Species composition and richness in temporary ponds were similar between drainage basins, although the fish assemblages in streams differed between basins. 4. Fish assemblage structure was influenced by local factors related to habitat structure, such as pond area and depth, canopy cover and hydroperiod. Physicochemical characteristics of the water in the ponds were similar between drainage basins and had little detectable effect on the structure of pond fish assemblages. 5. No correspondence was found between the composition, richness or abundance of fishes in the ponds and in stretches of the streams adjacent to the ponds. Therefore, it is not possible to predict the composition of these temporary pond fish assemblages from the fish assemblages found in adjacent streams.     

Variable salinity tolerance in ascidian larvae is primarily a plastic response to the parental environment

Both phenotypic plasticity and local genetic adaptation may contribute to a species’ ability to inhabit different environmental conditions. While phenotypic plasticity is usually considered costly, local adaptation takes generations to respond to environmental change and may be constrained by strong gene flow. The majority of marine species have complex life-cycles with pelagic stages that might be expected to promote gene flow and plastic responses, and yet several notable examples of local adaptation have been found in species with broadcast larvae. In the ascidian, Ciona intestinalis (Linnaeus, 1767),—a common marine species with broadcast spawning and a short larval stage—previous studies have found marked differences in salinity tolerance of early life-history stages among populations from different salinity regimes. We used common-garden experiments to test whether observed differences in salinity tolerance could be explained by phenotypic plasticity. Adult ascidians from two low salinity populations [2–5 m depth, ~25 practical salinity units (PSU)], and two full salinity populations (25–27 m depth, ~31 PSU) were acclimated for 2–4 weeks at both 25 and 31 PSU. Gametes were fertilized at the acclimation salinities, and the newly formed embryos were transferred to 10 different salinities (21–39 PSU) and cultured to metamorphosis. Adult acclimation salinity had an overriding and significant effect on larval metamorphic success: tolerance norms for larvae almost fully matched the acclimation salinity of the parents, independent of parental origin (deep or shallow). However we also detected minor population differences that could be attributed to either local adaptation or persistent environmental effects. We conclude that differences in salinity tolerance of C. intestinalis larvae from different populations are driven primarily by transgenerational phenotypic plasticity, a strategy that seems particularly favourable for an organism living in coastal waters where salinity is less readily predicted than in the open oceans.