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.     

Ontogeny of the hyobranchial apparatus in the salamanders Ambystoma talpoideum (Ambystomatidae) and Notophthalmus viridescens (Salamandridae): The ecological morphology of two neotenic strategies

Comparison of metamorphosis of skull and hyobranchial system in two species of neotenic salamanders reveals two different types of neoteny. Ambystoma talpoideum is completely neotenic owing to delayed metamorphosis. Notophthalmus viridescens exhibits limited neoteny as a result of incomplete metamorphosis. Morphological details of neoteny are compared to life history in both species in order to discuss the ecological morphology of the two neotenic strategies. Comparisons to Taricha granulosa, Triturus vulgaris, and Ambystoma gracile indicate that these two strategies are widely employed and may represent familial patterns.     

Speciation, phylogeography and evolution of life history and morphology in plethodontid salamanders of the Eurycea multiplicata complex

Understanding the complex interactions among environment, genotype and ontogeny in determining organismal phenotypes is cental to many biological disciplines. The Eurycea multiplicata complex, endemic to the Interior Highlands (Ozark Plateau and Ouachita Mountains) of eastern North America, comprises a diverse radiation of paedomorphic surface-dwelling (E. tynerensis), metamorphic surface-dwelling (E. multiplicata multiplicata and E. m. griseogaster) and metamorphic subterranean (Typhlotriton spelaeus) hemidactyliine plethodontid salamanders. Portions of two mitochondrial genes, cytochrome-b and NADH dehydrogenase-4, totalling 1818 base pairs (bp) were sequenced for 70 ingroup individuals plus numerous outgroup taxa, to examine the biogeography and relationships among these morphologically disparate species. Results show the E. multiplicata complex to be monophyletic, with its two most divergent clades corresponding to geography, not morphology or life history. Transforming surface-dwelling populations from the Ouachitas (E. m. multiplicata) are sister to the Ozark taxa, including paedomorphic surface-dwelling (E. tynerensis), subterranean (T. spelaeus) and transforming surface-dwelling salamanders assigned to the 'subspecies'E. m. griseogaster. Among Ozark taxa T. spelaeus (deeply nested within Eurycea) is sister to a clade that includes E. m. griseogaster and E. tynerensis. Current taxonomy suggests that paedomorphic populations (E. tynerensis) from the western Ozarks are distinct from nearby transforming populations (E. m. griseogaster). However, paedomorphic and transforming salamanders do not form reciprocally monophyletic groups and many populations share almost identical haplotypes. Ancestral state reconstruction of life history traits shows that paedomorphosis arose independently from three to nine times. Most populations are either completely paedomorphic or completely transforming. This suggests that local habitat parameters strongly influence life history mode in this complex, either facultatively or by selection for particular genotypes.     

EVOLUTION OF PAEDOMORPHOSIS IN PLETHODONTID SALAMANDERS: ECOLOGICAL CORRELATES AND RE‐EVOLUTION OF METAMORPHOSIS

Life‐history modes can profoundly impact the biology of a species, and a classic example is the dichotomy between metamorphic (biphasic) and paedomorphic (permanently aquatic) life‐history strategies in salamanders. However, despite centuries of research on this system, several basic questions about the evolution of paedomorphosis in salamanders have not been addressed. Here, we use a nearly comprehensive, time‐calibrated phylogeny of spelerpine plethodontids to reconstruct the evolution of paedomorphosis and to test if paedomorphosis is (1) reversible; (2) associated with living in caves; (3) associated with relatively dry climatic conditions on the surface; and (4) correlated with limited range size and geographic dispersal. We find that paedomorphosis arose multiple times in spelerpines. We also find evidence for re‐evolution of metamorphosis after several million years of paedomorphosis in a lineage of Eurycea from the Edwards Plateau region of Texas. We also show for the first time using phylogenetic comparative methods that paedomorphosis is highly correlated with cave‐dwelling, arid surface environments, and small geographic range sizes, providing insights into both the causes and consequences of this major life history transition.     

Geographic and genetic isolation in spring-associated Eurycea salamanders endemic to the Edwards Plateau region of Texas

Populations of neotenic, spring-associated salamanders of the genus Eurycea occupy discontinuous sites throughout the Edwards Plateau of central Texas and many warrant conservation attention. Here we used DNA sequence data from a nuclear (rag1) and a mitochondrial (ND4) gene to determine (1) the extent of genetic isolation among seven Edwards Plateau Eurycea populations and (2) the relationship between genetic distance and both geographic distance and hydrogeological features. Coalescent-based methods detected little gene flow among the sampled Eurycea populations, and we were unable to reject a model of complete isolation for any pair of populations. These findings were consistent with the relatively high genetic distances we detected among the sampled Eurycea populations (pairwise ϕ_ST ranged from 0.249 to 0.924). We detected a positive correlation between genetic distance and geographic distance, which is consistent with a pattern of isolation by distance. However, while controlling for geographic distance, we did not detect a positive relationship between genetic distance and aquifer or river distance. Thus, we found no evidence that aquifers and/or rivers serve as dispersal corridors among isolated Eurycea populations. Based on these results, we have no evidence that re-colonization of spring sites by migrant salamanders following local extirpation would be likely. Our findings indicate that spring-associated Eurycea salamander populations occupying the Edwards Plateau region are genetically isolated, and that each of these populations should be considered a distinct management unit.     

Predator Generalization Decreases the Effect of Introduced Predators in the San Marcos Salamander,Eurycea nana

The introduction of novel predators into an environment can have detrimental consequences on prey species, especially if these species lack the ability to recognize these predators. One such species that may be negatively affected by introduced predators is the federally threatened San Marcos salamander (Eurycea nana). Previous research found that predator‐naïve (captive‐hatched) salamanders showed decreased activity in response to the chemical cues of both a native fish predator (Micropterus salmoides) and an introduced fish predator (Lepomis auritus), but not to a non‐predatory fish (Gambusia geiseri). We tested the hypothesis that E. nana recognized the introduced Lepomis (and other non‐native Lepomis) because they share chemical cues with other native congeneric Lepomis predators in the San Marcos River. We examined the antipredator response of predator‐naïve E. nana to chemical cues from (1) a sympatric native sunfish (Lepomis cyanellus; Perciformes: Centrarchidae); (2) a sympatric introduced sunfish (L. auritus); (3) an allopatric sunfish (Lepomis gibbosus); (4) a sympatric non‐native, non‐centrarchid cichlid (Herichthys cyanoguttatum; Perciformes: Cichlidae); and (5) a blank water control to determine whether individuals make generalizations about novel predators within a genus and across a family. Exposure to chemical cues from all fish predator treatments caused a reduction in salamander activity (antipredator response). Additionally, there were no differences in the antipredator responses to each predatory fish treatment. The similar responses to all sunfish treatments indicate that E. nana shows predator generalization in response to novel predators that are similar to recognized predators. Additionally, the antipredator response to H. cyanoguttatum indicates that predator generalization can occur among perciform families.     

Intraguild predation among larval plethodontid salamanders: a field experiment in artificial stream pools

Intraguild predation can be important in determining community structure and dynamics. Artificial stream pools were used to test for the impacts of intraguild predation among three species of larval plethodontid salamanders. Intraguild predators (large Gyrinophilus porphyriticus and Pseudotriton ruber) significantly decreased the survival of small Pseudotriton ruber. There was a trend toward reduced growth of Pseudotriton and Eurycea cirrigera in the presence of intraguild predators. The presence of large Gyrinophilus significantly reduced the growth rate of large Pseudotriton, both in the absence and presence of intraguild prey. The presence of intraguild prey did not significantly increase the growth rates of the intraguild predators. Intraguild predation is likely to be an important force shaping the evolution and ecology of these salamanders.     

Computer-Assisted Photo Identification Outperforms Visible Implant Elastomers in an Endangered Salamander,Eurycea tonkawae

Despite recognition that nearly one-third of the 6300 amphibian species are threatened with extinction, our understanding of the general ecology and population status of many amphibians is relatively poor. A widely-used method for monitoring amphibians involves injecting captured individuals with unique combinations of colored visible implant elastomer (VIE). We compared VIE identification to a less-invasive method – computer-assisted photographic identification (photoID) – in endangered Jollyville Plateau salamanders (Eurycea tonkawae), a species with a known range limited to eight stream drainages in central Texas. We based photoID on the unique pigmentation patterns on the dorsal head region of 1215 individual salamanders using identification software Wild-ID. We compared the performance of photoID methods to VIEs using both ‘high-quality’ and ‘low-quality’ images, which were taken using two different camera types and technologies. For high-quality images, the photoID method had a false rejection rate of 0.76% compared to 1.90% for VIEs. Using a comparable dataset of lower-quality images, the false rejection rate was much higher (15.9%). Photo matching scores were negatively correlated with time between captures, suggesting that evolving natural marks could increase misidentification rates in longer term capture-recapture studies. Our study demonstrates the utility of large-scale capture-recapture using photo identification methods for Eurycea and other species with stable natural marks that can be reliably photographed.     

Histology of mental and caudal courtship glands in three genera of plethodontid salamanders (Amphibia: Plethodontidae)

Salamanders in the family Plethodontidae exhibit a unique tail‐straddle walk during courtship that can include the use of sexually dimorphic mental and caudal courtship glands. This study presents novel histological and fine structure data on mental glands and caudal courtship glands in Plethodon mississippi, Desmognathus conanti and Eurycea quadridigitata using both light microscopy and scanning electron microscopy. This study represents the first use of scanning electron microscopy to observe these glands. Both mental and caudal courtship glands were observed to vary seasonally in gland diameter and histology according to the breeding season of each species. Morphological variation was observed across the three species studied in both clustering and relative size of the glands compared to neighbouring mucous and granular glands. Hypertrophied mental glands are larger than mucous or granular glands in all species, but relationships among caudal courtship glands and other skin glands vary among species. In E. quadridigitata, active caudal courtship glands are larger than mucous and granular glands, but in D. conanti, caudal courtship glands are similar in size to granular glands and larger than mucous glands. In P. mississippi, caudal courtship glands are scattered among significantly larger granular glands and are similar in size to mucous glands.     

Interaction of an insecticide with larval density in pond-breeding salamanders (Ambystoma)

1. Amphibian populations residing in or near agricultural areas are often susceptible to pesticide contamination. Recent evidence suggests that the effects of pesticides on amphibians often exceed those estimated in laboratory toxicity tests because other environmental factors (e.g. predators, resource abundance) can influence pesticide toxicity. 2. To examine the effects of an insecticide (carbaryl) on two species of Ambystoma salamanders experiencing the natural stress of competition, we manipulated chemical concentration (control, 3.5 and 7.0 mg L^?1) and larval density (low and high). We determined the effect of treatments on snout‐vent length (SVL), growth rate, lipid reserves, time to metamorphosis, per cent survival and per cent metamorphosis. 3. Carbaryl negatively affected all response variables of Ambystoma maculatum significantly, and significantly reduced survival and metamorphosis of A. opacum. Increased density significantly influenced SVL, lipid reserves, growth rate and metamorphosis of A. maculatum. 4. The effects of carbaryl and increased density on per cent metamorphosis were nearly additive, but were generally less than additive on other variables. 5. The negative effects of chemical contamination on salamanders were likely because of pesticide‐induced reductions of food resources, as zooplankton abundance decreased by as much as 97% following carbaryl application. 6. Our study demonstrates the importance of the interactive effects that chemical contamination and natural environmental factors have on salamanders.     

Linking vertebral number to performance of aquatic escape responses in the axolotl (Ambystoma mexicanum)

Environmental conditions during early development in ectothermic vertebrates can lead to variation in vertebral number among individuals of the same species. It is often seen that individuals of a species raised at cooler temperatures have more vertebrae than individuals raised at warmer temperatures, although the functional consequences of this variation in vertebral number on swimming performance are relatively unclear. To investigate this relationship, we tested how vertebral number in axolotls (Ambystoma mexicanum) affected performance of aquatic escape responses (C-starts). Axolotls were reared at four temperatures (12–24 °C) encompassing their natural thermal range and then transitioned to a mean temperature (18 °C) three months before C-starts were recorded. Our results showed variation in vertebral number, but that variation was not significantly affected by developmental temperature. C-start performance among axolotls was significantly correlated with caudal vertebral number, and individuals with more caudal vertebrae were able to achieve greater curvature more quickly during their responses than individuals with fewer vertebrae. However, our results show that these individuals did not achieve greater displacements or velocities, and that developmental temperature did not have any effect on C-start performance. We highlight that the most important aspects of escape swim performance (i.e., how far individuals get from a threat and how quickly they move the most important parts of the body away from that threat) are consistent across individuals regardless of developmental temperature and morphological variation.     

Streambed microstructure predicts evolution of development and life history mode in the plethodontid salamander Eurycea tynerensis

Background

Habitat variation strongly influences the evolution of developmentally flexible traits, and may drive speciation and diversification. The plethodontid salamander Eurycea tynerensis is endemic to the geologically diverse Ozark Plateau of south-central North America, and comprises both strictly aquatic paedomorphic populations (achieving reproductive maturity while remaining in the larval form) and more terrestrial metamorphic populations. The switch between developmental modes has occurred many times, but populations typically exhibit a single life history mode. This unique system offers an opportunity to study the specific ecological circumstances under which alternate developmental and life history modes evolve. We use phylogenetic independent contrasts to test for relationships between a key microhabitat feature (streambed sediment) and this major life history polymorphism.

Results

We find streambed microstructure (sediment particle size, type and degree of sorting) to be highly correlated with life-history mode. Eurycea tynerensis is paedomorphic in streams containing large chert gravel, but metamorphoses in nearby streams containing poorly sorted, clastic material such as sandstone or siltstone.

Conclusion

Deposits of large chert gravel create loosely associated streambeds, which provide access to subsurface water during dry summer months. Conversely, streambeds composed of more densely packed sandstone and siltstone sediments leave no subterranean refuge when surface water dries, presumably necessitating metamorphosis and use of terrestrial habitats. This represents a clear example of the relationship between microhabitat structure and evolution of a major developmental and life history trait, and has broad implications for the role of localized ecological conditions on larger-scale evolutionary processes.     

Growth patterns of a stream vertebrate differ between urban and forested catchments

1. Urban development results in the decline of amphibian density and species richness. A logical next step towards understanding why urbanisation negatively impacts amphibians is to track species‐specific demographic responses to urbanisation. 2. We monitored growth of two‐lined salamander (Eurycea cirrigera Green) larvae over two complete cohorts (2006 and 2007) in nine western Georgia, U.S.A. streams. 3. We found that salamanders in streams surrounded by urbanised and developing catchments hatched at the same size as their reference‐stream counterparts, but achieved larger sizes within the first few months of growth. We evaluated the effect of four variables that correlate with the urban‐forest gradient and found that elevated temperatures in the urban environment, coupled with decreased intraspecific competition because of lower survivorship in these same habitats, were two of the most likely explanations for increased growth rates. 4. Such an increase in growth of surviving larvae may maintain population viability in urban areas where it has been shown survival is difficult because of increased in‐channel flow during flood events. Because larvae that do survive in urban streams undergo metamorphosis at large sizes, they may recoup a component of fitness (i.e. increased adult survivorship and reproduction) through growth.     

Larval salamanders and channel geomorphology are indicators of hydrologic permanence in forested headwater streams

Regulatory agencies need rapid indicators of hydrologic permanence for jurisdictional determinations of headwater streams. The study objective was to assess the utility of larval salamanders and habitat variables for determining stream permanence across a large geographic area. We sampled four core forests (61 sites in IN, KY, and OH) in spring (April–May) and summer (August–September) over a 2-year period. Sites in each forest were selected to cover a gradient of permanence, from perennial to ephemeral. Salamanders were collected by both benthic core sampling and timed visual search on each site visit. Classification and regression tree (CART) models were used to identify indicators of seasonal permanence at core sites that were then tested using data collected from 6 satellite forests (52 sites) located nationwide. Southern two-lined salamanders, Eurycea cirrigera, were numerically dominant and were the only species included in CART models. Salamander diversity declined with distance from the Appalachians and strong longitudinal changes in assemblage composition were evident within streams. Abundance of E. cirrigera was positively correlated with watershed area, whereas dusky salamanders, Desmognathus spp., and spring salamanders, Gyrinophilus porphyriticus, comprised a greater proportion of salamander communities at intermittent sites within their range. Spring and summer CART models incorporated E. cirrigera abundance and measures of channel geomorphology to accurately classify approximately 80% of core sites as either ephemeral, intermittent or perennial. When applied to validation data from national satellite forests, correct classification rates were >85% for intermittent and ephemeral sites, but were only ～20% for perennial sites. These findings suggest that larval plethodontid salamanders and habitat variables can be valuable predictors of headwater stream hydroperiod, but indicators are largely limited to the regional scale.     

Learning to Avoid Dangerous Habitat Types by Aquatic Salamanders,Eurycea tynerensis

There should be intense selection for predation avoidance mechanisms when prey live in close proximity to their predators. Prey individuals that can learn to associate habitat features with high levels of predation risk should experience increased survival if they subsequently avoid those habitats. We tested whether or not habitat learning occurred in a benthic stream community consisting of adult Oklahoma salamander (Eurycea tynerensis) prey and a syntopic predatory fish, the banded sculpin (Cottus carolinae). We exposed individual salamanders to chemical stimuli from sculpin, non‐predatory tadpoles, or a blank control in training tanks containing either rocks or grass. Two days later, the salamanders were tested in tanks that offered a choice of rocks or grass. Salamanders showed significant avoidance of the habitat where they had previously encountered chemical cues from sculpin in comparison to the non‐predatory controls. Learning to avoid dangerous habitats may be particularly important for prey whose predators are visually cryptic ambush foragers, such as sculpin.     

Diet composition of two larval headwater stream salamanders and spatial distribution of prey

相似文献   

A New Species of Eimeria (Apicomplexa: Eimeriidae) from the marbled salamander, Ambystoma opacum (Caudata: Ambystomatidae), from northern Louisiana

Between December 2002 and June 2004, 10 marbled salamanders, Ambystoma opacum, were examined for coccidian parasites. Salamanders were collected in Bradley (n = 2), Little River (n = 1), Miller (n = 1), and Sevier (n = 1) Counties, Arkansas; Webster Parish, Louisiana (n = 2); and Bowie (n = 1) and Nacogdoches (n = 2) Counties, Texas. Two of 10 (20%) A. opacum from Louisiana harbored an undescribed species of Eimeria. Oocysts of Eimeria trauthi n. sp. were ellipsoidal, 36.6 x 33.1 (33-40 x 29-37) microm, with a thin, single-layered wall; shape index 1.1. Polar granule(s) and micropyle were absent. Oocyst residuum was composed of hundreds of loosely packed homogenous granules of various sizes enclosing a vacuole. Sporocysts were elongate-ellipsoidal, 20.8 x 8.1 (19-22 x 7-9) microm; shape index 2.6. Sporocyst residuum was spherical and composed of a cluster of granules often membrane-bound. This is the first time a coccidium has been reported from an amphibian species in Louisiana and the second time a coccidium has been described from this salamander host. In addition, the following 26 salamanders from various counties in Arkansas, Oklahoma, and Texas were surveyed during the study period and were negative for coccidia: Ambystomatidae, 4 spotted salamanders (Ambystoma maculatum) and 7 mole salamanders (Ambystoma talpoideum); Cryptobranchidae, 4 Ozark hellbenders (Cryptobranchus alleganiensis bishopi); Plethodontidae, 6 spotted dusky salamanders (Desmognathus conanti) and 3 many-ribbed salamanders (Eurycea multiplicata multiplicata); and Salamandridae, 2 central newts (Notophthalmus viridescens louisianensis).