Life history plasticity does not confer resilience to environmental change in the mole salamander (<Emphasis Type="Italic">Ambystoma talpoideum)</Emphasis>

Plasticity in life history strategies can be advantageous for species that occupy spatially or temporally variable environments. We examined how phenotypic plasticity influences responses of the mole salamander, Ambystoma talpoideum, to disturbance events at the St. Marks National Wildlife Refuge (SMNWR), FL, USA from 2009 to 2014. We observed periods of extensive drought early in the study, in contrast to high rainfall and expansive flooding events in later years. Flooding facilitated colonization of predatory fishes to isolated wetlands across the refuge. We employed multistate occupancy models to determine how this natural experiment influenced the occurrence of aquatic larvae and paedomorphic adults and what implications this may have for the population. We found that, in terms of occurrence, responses to environmental variation differed between larvae and paedomorphs, but plasticity (i.e. the ability to metamorphose rather than remain in aquatic environment) was not sufficient to buffer populations from declining as a result of environmental perturbations. Drought and fish presence negatively influenced occurrence dynamics of larval and paedomorphic mole salamanders and, consequently, contributed to observed short-term declines of this species. Overall occurrence of larval salamanders decreased from 0.611 in 2009 to 0.075 in 2014 and paedomorph occurrence decreased from 0.311 in 2009 to 0.121 in 2014. Although variation in selection pressures has likely maintained this polyphenism previously, our results suggest that continued changes in environmental variability and the persistence of fish in isolated wetlands could lead to a loss of paedomorphosis in the SMNWR population and, ultimately, impact regional persistence in the future.     

Paedomorphosis in <Emphasis Type="Italic">Ambystoma talpoideum</Emphasis>: effects of initial body size variation and density

Facultative paedomorphosis is the ability of a salamander to either metamorphose into a terrestrial, metamorphic adult or retain a larval morphology to become a sexually mature paedomorphic adult. It has been hypothesized that density and initial body size variation within populations are instrumental in cueing metamorphosis or paedomorphosis in salamanders, yet few studies have adequately tested these hypotheses in long-term experiments. Beginning in the spring of 2004, 36 experimental ponds were used to manipulate three body size variation levels (low, medium, high) and two density levels (low, high) of Ambystoma talpoideum larvae. Larvae were individually marked using visible implant elastomers and collected every 2 weeks in order to measure snout–vent length and mass. Bi-nightly sampling was used to collect new metamorphs as they appeared. Analysis revealed significant effects of density, size variation and morph on body size of individuals during the summer. Individuals that metamorphosed during the fall and following spring were significantly larger as larvae than those becoming paedomorphic across all treatments. These results support the Best-of-a-Bad-Lot hypothesis, which proposes that the largest larvae metamorphose in order to escape unfavorable aquatic habitats. Large larvae may metamorphose to leave aquatic habitats, regardless of treatment, due to the colder climate and lower productivity found in Kentucky, which is in the northern-most part of A. talpoideum’s range. By maintaining a long-term experiment, we have provided evidence for the transition of both larvae and paedomorphs into metamorphs during fall and spring metamorphosis events. Furthermore, the production of similar morphs under different environmental conditions observed in this research suggests that the ecological mechanisms maintaining polyphenisms may be more diverse that first suspected. Electronic supplementary material The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Growth and foraging consequences of facultative paedomorphosis in the tiger salamander,Ambystoma tigrinum nebulosum

Summary Facultative paedomorphosis in salamanders occurs when larvae respond to varying environmental conditions by either metamorphosing into terrestrial metamorphic adults or retaining their larval morphology to become sexually mature paedomorphic adults. Several hypotheses have been proposed for the evolutionary maintenance of this environmentally induced dimorphism, but few data are available to assess them adequately. We studied a montane population of the tiger salamander,Ambystoma tigrinum nebulosum, and measured the adult growth rate and body condition across three growing seasons to assess the relative costs and benefits of each morph. Metamorphic adults grew more than paedomorphic adults in terms of snout—vent length across years and in weight within years. Dietary analyses and foraging experiments revealed some of the proximate factors that may underlie these differential growth patterns. Across all prey, metamorphs had significantly higher biomass and calories per stomach sample than paedomorphs. Metamorphic diets primarily consisted of the fairy shrimpBranchinecta coloradensis, whereas paedomorphic diets contained a variety of benthic and terrestrial invertebrates. Foraging experiments revealed that both morphs are more successful at capturing fairy shrimp relative to other prey types and both show high electivity toward this prey. However, fairy shrimp occurred only in non-permanent ponds and thus are inaccessible to paedomorphs, which can survive only in permanent ponds. Paedomorphs also experience higher levels of intraspecific competition with large larvae in permanent ponds than metamorphs do in non-permanent ponds. Thus, metamorphs obtain a growth advantage over paedomorphs by foraging in non-permanent ponds that contain fairy shrimp and have reduced intraspecific competition. These results suggest that paedomorphs should have decreased fitness relative to metamorphs, primarily because metamorphs can move into the best habitats for growth. The net fitness effect of morph-specific differences in dispersal depend on whether there are trade-offs with other life history traits. Nonetheless, because the relative benefit of metamorph dispersal will change with environmental conditions in permanent ponds and the surrounding habitat, the relative fitness payoff to each morph should track changes in the environment. Thus, facultative paedomorphosis may be maintained in part by variable, environmentally-specific fitness payoffs to each morph.     

Facultative paedomorphosis as a mechanism promoting intraspecific niche differentiation

Organisms with complex life cycles are characterized by a metamorphosis that allows for a major habitat shift and the exploitation of alternative resources. However, metamorphosis can be bypassed in some species through a process called paedomorphosis, resulting in the retention of larval traits at the adult stage and is considered important at both micro‐ and macroevolutionary scales. In facultatively paedomorphic populations of newts, some individuals retain gills and a fully aquatic life at the adult stage (paedomorphs), while others undergo complete metamorphosis (metamorphs), allowing for a terrestrial life‐stage. Because facultative paedomorphosis affects trophic structures and feeding mechanism of newts, one hypothesis is that it may be maintained as a trophic polymorphism, with the advantage to lessen intraspecific competition during the shared aquatic life‐stage. Here, we tested this hypothesis combining stomach content data with stable isotope techniques, using carbon and nitrogen stable isotopes, in facultatively paedomorphic alpine newts Ichthyosaura alpestris. Both stomach content and stable isotope analyses showed that paedomorphs had smaller trophic niches and were more reliant on pelagic resources, while metamorphs relied more on littoral resources, corresponding to a polyphenism along the littoral–pelagic axis and the extension of the population's trophic niche to otherwise ‘underused’ pelagic resources by paedomorphs. Interestingly, stable isotopes revealed that the trophic polyphenism was less marked in males than in females and potentially linked to sexual activity. Although paedomorphosis and metamorphosis are primarily seen as results of tradeoffs between the advantages of using aquatic versus terrestrial habitats, this study provides evidence that additional forces, such as intraspecific trophic niche differences between morphs and trophic niche expansion, may play an important role in the persistence of this dimorphism in heterogeneous environments. Moreover, the different patterns found in males and females show the importance of considering sex to understand the evolutionary ecology of trophic polymorphisms.     

Genetic structure of lake and stream populations in a Pyrenean amphibian (Calotriton asper) reveals evolutionary significant units associated with paedomorphosis

Differences in environmental conditions such as those between lakes and streams can produce phenotypic variation and ultimately promote evolutionary diversification. Some species of newts and salamanders can occupy these habitats and express alternative phenotypes: metamorphs that lose gills at metamorphosis and paedomorphs that retain them at the adult stage. Whereas this process is facultative in some species, it is obligatory in others, thus suggesting that isolation and environmental pressures may have canalized developmental pathways. In this study, we focused our research on the Pyrenean brook newt, Calotriton asper, which is present in both lakes and streams, but whose fully aquatic paedomorphic individuals are only present in lakes. We aimed to determine the genetic structure and differentiation of two paedomorphic populations, including their surrounding stream and lake metamorphic populations, to test whether populations of paedomorphs can constitute evolutionary significant units. Although gene flow was identified between lakes and nearby stream populations, there was a low percentage of dispersers, and the paedomorphic populations were genetically differentiated from the populations of metamorphs. It is likely that the studied lakes have offered peculiar conditions that have allowed the development of a paedomorphic phenotype. These populations and phenotypes therefore constitute good models to understand local adaptations. As each of these populations of paedomorphs can be considered evolutionary significant units that cannot be replaced by other nearby populations in case of a population crash, conservation actions should be focused directly on them.     

Are direct density cues,not resource competition,driving life history trajectories in a polyphenic salamander?

Polyphenisms, where multiple, discrete, environmentally-cued phenotypes can arise from a single genotype, are extreme forms of phenotypic plasticity. Cue acquisition and interpretation are vital for matching phenotypes to varying environments, but can be difficult if cues are unreliable indicators or if multiple cues are present simultaneously. Facultative paedomorphosis, where juvenile traits are retained at sexual maturity, is a density-dependent polyphenism exhibited by many salamanders. Favorable conditions such as low larval densities and stable hydroperiod delay metamorphosis and promote a paedomorphic strategy. We investigated proximate cues affecting facultative paedomorphosis in order to understand how larval newts (Notophthalmus viridescens louisianensis) assess conspecific density. To isolate the effects of density cues from the effects of resources and agonistic behavior, we caged larval newts in mesocosms in a 2?×?2 factorial design that manipulated both background larval newt densities (high or low) and food levels (ambient or supplemented). We found strong effects of both food and density on caged individuals. Under high densities, caged larvae were more likely to become efts, a long-lasting juvenile terrestrial stage, across both food levels, while paedomorphs were more common under low densities. Though food levels increased growth rates, density had strong independent effects on metamorphic timing and phenotype. Competition for food and space are classical density-dependent processes, but density cues themselves may be a mediator of density-dependent effects on polyphenisms and life history responses.     

How do paedomorphic newts cope with lake drying?

Paedomorphosis, in which adult individuals retain larval traits, is widespread in newts and salamanders. Most evolutionary models predict the maintenance of this life-history trait in favourable aquatic habitats surrounded by hostile terrestrial environments. Nevertheless, numerous ponds inhabited by paedomorphic individuals are unpredictable and temporary. In an experimental framework, I showed that paedomorphic newts were able to metamorphose and thus survive in the absence of water. However, the mere decrease of water level or the life space do not seem to induce metamorphosis in paedomorphs. On the contrary, drying up induces almost all individuals to move on land and after that to colonize other aquatic sites located nearby. Such terrestrial migrations allow survival in drying conditions without metamorphosis as long as the distances of terrestrial migration are short. These results are consistent with the presence of paedomorphs in drying ponds and are in favor of classic optimality models predicting metamorphosis in unfavorable environments.     

Evolutionary ecology of facultative paedomorphosis in newts and salamanders

Facultative paedomorphosis is an environmentally induced polymorphism that results in the coexistence of mature, gilled, and fully aquatic paedomorphic adults and transformed, terrestrial, metamorphic adults in the same population. This polymorphism has been of interest to scientists for decades because it occurs in a large number of caudate amphibian taxa as well as in a large diversity of habitats. Numerous experimental and observational studies have been conducted to explain the proximate and ultimate factors affecting these heterochronic variants in natural populations. The production of each alternative phenotype is based on a genotypexenvironment interaction and research suggests that differences in the environment can produce paedomorphs through several ontogenetic pathways. No single advantage accounts for the maintenance of this polymorphism. Rather, the interplay of different costs and benefits explains the success of the polyphenism across variable environments. Facultative paedomorphosis allows individuals to cope with habitat variation, to take advantage of environmental heterogeneity in the presence of open niches, and to increase their fitness. This process is expected to constitute a first step towards speciation events, and is also an example of biodiversity at the intraspecific level. The facultative paedomorphosis system is thus ripe for future studies encompassing ecology, evolution, behaviour, endocrinology, physiology, and conservation biology. Few other systems have been broad enough to provide varied research opportunities on topics as diverse as phenotypic plasticity, speciation, mating behaviour, and hormonal regulation of morphology. Further research on facultative paedomorphosis will provide needed insight into these and other important questions facing biologists.     

Terrestriality constrains salamander limb diversification: Implications for the evolution of pentadactyly

Patterns of phenotypic evolution can abruptly shift as species move between adaptive zones. Extant salamanders display three distinct life cycle strategies that range from aquatic to terrestrial (biphasic), to fully aquatic (paedomorphic) and to fully terrestrial (direct development). Life cycle variation is associated with changes in body form such as loss of digits, limb reduction or body elongation. However, the relationships among these traits and life cycle strategy remain unresolved. Here, we use a Bayesian modelling approach to test whether life cycle transitions by salamanders have influenced rates, optima and integration of primary locomotory structures (limbs and trunk). We show that paedomorphic salamanders have elevated rates of limb evolution with optima shifted towards smaller size and fewer digits compared to all other salamanders. Rate of hindlimb digit evolution is shown to decrease in a gradient as life cycles become more terrestrial. Paedomorphs have a higher correlation between hindlimb digit loss and increases in vertebral number, as well as reduced correlations between limb lengths. Our results support the idea that terrestrial plantigrade locomotion constrains limb evolution and, when lifted, leads to higher rates of trait diversification and shifts in optima and integration. The basic tetrapod body form of most salamanders and the independent losses of terrestrial life stages provide an important framework for understanding the evolutionary and developmental mechanisms behind major shifts in ecological zones as seen among early tetrapods during their transition from water to land.     

Life cycle polyphenism as a factor affecting ecological divergence within <Emphasis Type="Italic">Notophthalmus viridescens</Emphasis>

Polyphenism, which allows a single genotype to express multiple discrete phenotypes in response to environmental cues, is an adaptive trait in heterogeneous environments. Pond hydroperiod is an important ecological parameter affecting amphibian life history, and variation in local pond hydrology has been hypothesized to play a role in species divergence via changes in polyphenism. The eastern newt (Notophthalmus viridescens) expresses life cycle polyphenism. Larvae develop along three possible pathways: metamorphosis to aquatic lunged adult via a terrestrial juvenile (eft) stage, metamorphosis directly to an aquatic lunged adult, or maturation directly to an aquatic gilled adult without metamorphosis (i.e., paedomorphosis). Subspecies of N. viridescens vary in their polyphenic patterns, suggesting possible adaptation to different environments. However, no studies have experimentally tested how genetic and environmental components contribute to the observed differences among subspecies and whether such differences may facilitate divergence. We tested whether adaptation to local pond hydrology via polyphenic changes existed among subspecies by rearing larvae of three subspecies (N. v. dorsalis, N. v. louisianensis, and N. v. viridescens) along three hydroperiod regimes (short, long, and constant) in outdoor artificial ponds. We found that larval N. v. viridescens obligately metamorphosed to efts under all hydroperiods, whereas N. v. dorsalis and N. v. louisianensis exhibited plasticity: larvae metamorphosed to efts under drying conditions but metamorphosed directly to aquatic adults or became paedomorphic in constant water. Also, N. v. viridescens metamorphosed to efts faster and at a smaller body size than the other two subspecies. These data suggest that subspecies of N. viridescens are adapted to different pond hydroperiods, supporting the potential for polyphenism to facilitate divergence. Canalizing selection for certain alternative phenotypes within a single species in which other populations remain plastic may play an important role in the initiation of ecological divergence.     

Seasonal variation of morph ratio in facultatively paedomorphic populations of the palmate newt Triturus helveticus

Facultative paedomorphosis is a polyphenism in which individuals may express one of two alternative ontogenetic pathways (metamorphosis vs. paedomorphosis) depending on environmental cues. Previous laboratory experiments showed that drying can cause morph ratio change, suggesting that the maintenance of facultative paedomorphosis is highly dependent on environmental determinants. The aim of this study was to examine seasonal variation in morph ratios in eight ponds from Larzac (southern France) naturally inhabited by palmate newts and to relate it to pond drying. In some ponds, the relative proportion of paedomorphs (i.e. individuals retaining gills at the adult stage) increased after the breeding period, but it remained stable or decreased in other ponds. This seasonal variation in the abundance of the two morphs most probably reflects (1) the emigration of metamorphs leaving the pond to occupy terrestrial habitats and (2) metamorphosis of paedomorphic adults in response to drying of the ponds. This study shows that facultative paedomorphosis in palmate newts is a dynamic process that allows rapid change (i.e. within a single year) in morph ratio to fit environmental variation (i.e. risk of drying) within the aquatic habitats. Long-term studies are needed to model the evolution of the dimorphism according to environmental change.     

Filling ephemeral ponds affects development and phenotypic expression in Ambystoma talpoideum

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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.     

Predation and the relative importance of larval colour polymorphisms and colour polyphenism in a damselfly

Intraspecific body colour variation is common in many animal species. Predation could be a key selective agent giving rise to variation in body colour, and such variation could be due to genetics (polymorphisms) or phenotypic plasticity (polyphenisms). In this study we examined the degree of colour polymorphism and polyphenism in background colour matching in larvae of the damselfly Coenagrion armatum. In addition, we tested if predation risk is reduced when larvae are exposed to a matching compared to a non-matching background. By raising families of larvae at three different background colours we showed that polymorphism explained about 20 % of the total variation and polyphenism about 35 %. In a predation experiment with fish, we showed that larvae with a body colour matching the background had a higher survival success compared to larvae with a non-matching background colour. We suggest that the background matching is adaptive in terms of survival from predation and that colour diversity is maintained because of spatial and temporal variation in the background experienced by damselfly larvae under field conditions.     

Thyroid hormone responsive QTL and the evolution of paedomorphic salamanders

The transformation of ancestral phenotypes into novel traits is poorly understood for many examples of evolutionary novelty. Ancestrally, salamanders have a biphasic life cycle with an aquatic larval stage, a brief and pronounced metamorphosis, followed by a terrestrial adult stage. Repeatedly during evolution, metamorphic timing has been delayed to exploit growth-permissive environments, resulting in paedomorphic salamanders that retain larval traits as adults. We used thyroid hormone (TH) to rescue metamorphic phenotypes in paedomorphic salamanders and then identified quantitative trait loci (QTL) for life history traits that are associated with amphibian life cycle evolution: metamorphic timing and adult body size. We demonstrate that paedomorphic tiger salamanders (Ambystoma tigrinum complex) carry alleles at three moderate effect QTL (met1–3) that vary in responsiveness to TH and additively affect metamorphic timing. Salamanders that delay metamorphosis attain significantly larger body sizes as adults and met2 explains a significant portion of this variation. Thus, substitution of alleles at TH-responsive loci suggests an adaptive pleiotropic basis for two key life-history traits in amphibians: body size and metamorphic timing. Our study demonstrates a likely pathway for the evolution of novel paedomorphic species from metamorphic ancestors via selection of TH-response alleles that delay metamorphic timing and increase adult body size.     

Biochemical plasticity in the Arizona tiger salamander (Ambystoma tigrinum nebulosum).

The Arizona tiger salamander, Ambystoma tigrinum nebulosum, is a developmentally polymorphic species. Some individuals become sexually mature while retaining some larval traits (paedomorphs), while other individuals mature as metamorphosed salamanders. In this study, relative enzyme activities of the products of two duplicate loci in each of three enzyme systems (aconitase, malate dehydrogenase, and isocitrate dehydrogenase) were measured in paedomorphs and in paedomorphs forced to metamorphose by treatment with thyroxine. We found that thyroxine and laboratory conditions affect enzyme activities of four of the six enzymes examined and that activities of products of duplicate loci are altered to different degrees.     

Temperature sex-reversal in amphibians and reptiles

The sexual differentiation of gonads has been shown to be temperature-sensitive in many species of amphibians and reptiles. In two close species of salamanders, Pleurodeles poireti and P. waltl, both displaying a ZZ/ZW mechanism of genotypic sex determination (GSD), the rearing of larvae at high temperatures (30 degrees-32 degrees C) produces opposite effects: ZZ genotypic males of Pleurodeles poireti become phenotypic females whereas ZW genotypic females of P. waltl become phenotypic males. Sex-reversal of these individuals has been irrefutably demonstrated through genetic, cytogenetic, enzymatic and immunological studies. In many turtles, both sexes differentiate only within a critical range of temperature: above this range, all the individuals become phenotypic females, whereas below it, 100% become phenotypic males. The inverse occurs in some crocodiles and lizards. In many species of these three orders of reptiles, females are obtained at low and high temperatures, and males at intermediate ones. Preliminary studies in turtles (Emys orbicularis) indicate that within the critical range of temperature, sexual phenotype conforms with GSD, but that above and below this range, GSD is overriden. Temperature shifts during larval development in salamanders and during embryonic development in reptiles allowed the determination of thermosensitive stages for gonadal differentiation. Estrogens synthesized in the gonads at these stages appear to be involved in their sexual differentiation, higher levels being produced at feminizing temperatures than at masculinizing ones. The phenomenon of temperature sensitivity of gonadal differentiation occurs in species showing a very early stage in the evolution of sex chromosomes. Its adaptive value, chiefly in reptiles, remains an open question.     

Candidate gene analysis of metamorphic timing in ambystomatid salamanders

Although much is known about the ecological significance of metamorphosis and metamorphic timing, few studies have examined the underlying genetic architecture of these traits, and no study has attempted to associate phenotypic variation to molecular variation in specific genes. Here we report on a candidate gene approach (CGA) to test specific loci for a statistical contribution to variation in metamorphic timing. Three segregating populations (SP1, SP2 and SP3) were constructed utilizing three species of paedomorphic Mexican ambystomatid salamander, including the axolotl, Ambystoma mexicanum. We used these replicated species to test the hypothesis that inheritance of alternate genotypes at two thyroid hormone receptor loci (TRalpha, TRbeta) affects metamorphic timing in ambystomatid salamanders. A significant TRalpha*SP effect indicated that variation in metamorphic timing may be influenced by TRalpha genotype, however, the effect was not a simple one, as both the magnitude and direction of the phenotypic effect depended upon the genetic background. These are the first data to implicate a specific gene in contributing to variation in metamorphic timing. In general, candidate gene approaches can be extended to any number of loci and to any organism where simple genetic crosses can be performed to create segregating populations. The approach is thus of particular value in ecological studies where target genes have been identified but the study organism is not one of the few well-characterized model systems that dominate genetic research.     

Morph switching in a dimorphic population of <Emphasis Type="Italic">Triturus alpestris</Emphasis> (Amphibia,Caudata)

The usual life cycle of Alpine newts comprises an aquatic larval stage and a terrestrial juvenile and adult stage. However, some populations differ from this pattern in exhibiting facultative paedomorphosis where some individuals reach sexual maturity while retaining larval traits such as gills and gill slits. While paedomorphic newts can, in some circumstances, initiate metamorphosis, once a newt has commenced metamorphosis, the state is irreversible. Because the frequency of this switching from one morph to the other has never been quantified in the wild, we attempted to estimate switching rate and survival by carrying out a 3-year monitoring survey of a population inhabiting an alpine lake. While morph switching did occur in this population, it involved a relatively low proportion of the paedomorphs (approx. 12%), suggesting that metamorphosis is not favoured in the study population. The hypothesis of paedomorphic advantage was not supported since neither survival nor body condition differed between morphs. The ontogenetic pathway of wild Alpine newts is thus characterised by two forks in the developmental pathway. The first occurs during the larval stage (metamorphosis vs. paedomorphosis), and the second occurs in paedomorphic adults (switching for metamorphosis vs. continuation of the paedomorphic lifestyle). Such a two-level decision process may allow individuals to cope with environmental uncertainty.