Polyphenism predicts actuarial senescence and lifespan in tiger salamanders.

Actuarial senescence (called 'senescence' hereafter) often shows broad variation at the intraspecific level. Phenotypic plasticity likely plays a central role in among-individual heterogeneity in senescence rate (i.e. the rate of increase in mortality with age), although our knowledge on this subject is still very fragmentary. Polyphenism-the unique sub-type of phenotypic plasticity where several discrete phenotypes are produced by the same genotype-may provide excellent study systems to investigate if and how plasticity affects the rate of senescence in nature. In this study, we investigated whether facultative paedomorphosis influences the rate of senescence in a salamander, Ambystoma mavortium nebulosum. Facultative paedomorphosis, a unique form of polyphenism found in dozens of urodele species worldwide, leads to the production of two discrete, environmentally induced phenotypes: metamorphic and paedomorphic individuals. We leveraged an extensive set of capture-recapture data (8948 individuals, 24 years of monitoring) that were analysed using multistate capture-recapture models and Bayesian age-dependent survival models. Multistate models revealed that paedomorphosis was the most common developmental pathway used by salamanders in our study system. Bayesian age-dependent survival models then showed that paedomorphs have accelerated senescence in both sexes and shorter adult lifespan (in females only) compared to metamorphs. In paedomorphs, senescence rate and adult lifespan also varied among ponds and individuals. Females with good body condition and high lifetime reproductive success had slower senescence and longer lifespan. Late-breeding females also lived longer but showed a senescence rate similar to that of early-breeding females. Moreover, males with good condition had longer lifespan than males with poor body condition, although they had similar senescence rates. In addition, late-breeding males lived longer but, unexpectedly, had higher senescence than early-breeding males. Overall, our work provides one of the few empirical cases suggesting that environmentally cued polyphenism could affect the senescence of a vertebrate in nature, thus providing insights on the ecological and evolutionary consequences of developmental plasticity on ageing.

The role of environmental variation in mediating fitness trade-offs for an amphibian polyphenism.

Fitness trade-offs are a foundation of ecological and evolutionary theory because trade-offs can explain life history variation, phenotypic plasticity, and the existence of polyphenisms. Using a 32-year mark-recapture dataset on lifetime fitness for 1093 adult Arizona tiger salamanders (Ambystoma mavortium nebulosum) from a high elevation, polyphenic population, we evaluated the extent to which two life history morphs (aquatic paedomorphs vs. terrestrial metamorphs) exhibited fitness trade-offs in breeding and body condition with respect to environmental variation (e.g. climate) and internal state-based variables (e.g. age). Both morphs displayed a similar response to higher probabilities of breeding during years of high spring precipitation (i.e. not indicative of a morph-specific fitness trade-off). There were likely no climate-induced fitness trade-offs on breeding state for the two life history morphs because precipitation and water availability are vital to amphibian reproduction. Body condition displayed a contrasting response for the two morphs that was indicative of a climate-induced fitness trade-off. While metamorphs exhibited a positive relationship with summer snowpack conditions, paedomorphs were unaffected. Fitness trade-offs from summer snowpack are likely due to extended hydroperiods in temporary ponds, where metamorphs gain a fitness advantage during the summer growing season by exploiting resources that are unavailable to paeodomorphs. However, paedomorphs appear to have the overwintering fitness advantage because they consistently had higher body condition than metamorphs at the start of the summer growing season. Our results reveal that climate and habitat type (metamorphs as predominately terrestrial, paedomorphs as fully aquatic) interact to confer different advantages for each morph. These results advance our current understanding of fitness trade-offs in this well-studied polyphenic amphibian by integrating climate-based mechanisms. Our conclusions prompt future studies to explore how climatic variation can maintain polyphenisms and promote life history diversity, as well as the implications of climate change for polyphenisms.

Current and lagged climate affects phenology across diverse taxonomic groups.

The timing of life events (phenology) can be influenced by climate. Studies from around the world tell us that climate cues and species' responses can vary greatly. If variation in climate effects on phenology is strong within a single ecosystem, climate change could lead to ecological disruption, but detailed data from diverse taxa within a single ecosystem are rare. We collated first sighting and median activity within a high-elevation environment for plants, insects, birds, mammals and an amphibian across 45 years (1975-2020). We related 10 812 phenological events to climate data to determine the relative importance of climate effects on species' phenologies. We demonstrate significant variation in climate-phenology linkage across taxa in a single ecosystem. Both current and prior climate predicted changes in phenology. Taxa responded to some cues similarly, such as snowmelt date and spring temperatures; other cues affected phenology differently. For example, prior summer precipitation had no effect on most plants, delayed first activity of some insects, but advanced activity of the amphibian, some mammals, and birds. Comparing phenological responses of taxa at a single location, we find that important cues often differ among taxa, suggesting that changes to climate may disrupt synchrony of timing among taxa.

Experimental warming reduces body mass but not reproductive investment.

Climate change has already had wide-ranging effects on populations, including shifts in species' ranges, phenology, and body size. Whereas some common patterns have emerged, the direction and magnitude of responses vary extensively among populations as well as across life stages within populations. Understanding the consequences of climate change and predicting future responses at the population level require experimental tests of how warmer temperatures affect life history traits, including growth rate, development time, and reproductive output. Here, we tested how experimental warming affected life history from larval development and survival to adult reproductive maturity and investment in mole salamanders, Ambystoma talpoideum. We found that a small temperature increase (~1°C) experienced during larval development had complex consequences: density-dependent effects on growth and body mass, density-independent effects on fat storage, and no effects on survival and reproductive investment. Although warming reduced growth rates, size at maturity, and fat storage, salamanders in both warmed and control conditions had similar survival and reproductive investment in their first year. However, costs of smaller body size and lower fat reserves may limit overwintering survival and/or future reproduction. Our study highlights the differential effects of warming across life history traits and multifaceted population responses to climate change. This work motivates future studies to examine variation in response to climate change across life stages and life history traits.

Extending the biologging revolution to amphibians: Implantation, extraction, and validation of miniature temperature loggers.

Quantifying ectotherm body temperature is important to understand physiological performance under environmental change. The increasing availability of small, commercially-available animal-borne biologgers increases accessibility to high-quality body temperature data. However, amphibians present several challenges to successful datalogger implantation including small body sizes and physiologically active skin. We developed a method for the implantation, extraction, and validation of temperature biologgers in captive salamanders. We assessed the effect of biologger implantation and extraction surgery on body condition. Implantation had no effects on short or long-term body condition. Body condition also did not differ between implant and control groups after datalogger extraction. Biologgers did not alter preferred temperature in a laboratory thermal gradient, indicating that temperature data would not be biased by implantation. We provide detailed recommendations for datalogger placement and refinement of surgical techniques to further improve outcomes, enhance our understanding of fitness, species range limitations, and responses to environmental and climatic change.

Omnivore density affects community structure through multiple trophic cascades.

Omnivores can dampen trophic cascades by feeding at multiple trophic levels, yet few studies have evaluated how intraspecific variation of omnivores influences community structure. The speckled dace (Rhinichthys osculus) is a common and omnivorous minnow that consumes algae and invertebrates. We studied effects of size and size structure on top-down control by dace and how effects scaled with density. Dace were manipulated in a mesocosm experiment and changes in invertebrate and algal communities and ecosystem function were monitored. Omnivores affected experimental communities via two distinct trophic pathways (benthic and pelagic). In the benthic pathway, dace reduced macroinvertebrate biomass, thereby causing density-mediated indirect effects that led to increased benthic algal biomass. Dace also reduced pelagic predatory macroinvertebrate biomass (hemipterans), thereby increasing the abundance of emerging insects. The effect of dace and hemipterans on emerging insects was mediated by a non-linear response to dace with peak emergence at intermediate dace density. In contrast with recent studies, omnivore size and size structure had no clear effect, indicating that small and large dace in our experiment shared similar functional roles. Our results support that the degree to which omnivores dampen trophic cascades depends on their relative effect on multiple trophic levels, such that the more omnivorous a predator is, the more likely cascades will be dampened. Availability of abundant macroinvertebrates, and the absence of top predators, may have shifted dace diets from primary to secondary consumption, strengthening density-dependent trophic cascades. Both omnivore density and dietary shifts are important factors influencing omnivore-mediated communities.

Relative size underlies alternative morph development in a salamander.

Size thresholds commonly underlie the induction of alternative morphological states. However, the respective importance of absolute and relative size to such thresholds remains uncertain. If absolute size governs expression, morph frequency should differ among environments that influence absolute sizes (e.g. resources, competition), and individuals of the same morph should have similar average sizes across environments. If relative size determines expression, the frequency of each morph may not differ among environments, but morphs within each environment should differ in size relative to one another. We tested these predictions in a salamander (Ambystoma talpoideum) that develops into either a terrestrial metamorph or an aquatic paedomorph. To generate size variation within and among environments, we reared individuals in mesocosm ponds across three conspecific densities. We found that morph frequency did not differ among density treatments, and the morphs were not similarly sized within each density treatment. Instead, within each environment, relatively larger individuals became metamorphs and relatively smaller individuals became paedomorphs. Relative size therefore determined morph development, highlighting the importance of an individual's social context to size-dependent morph induction.

Lifetime Fitness, Sex-Specific Life History, and the Maintenance of a Polyphenism.

Polyphenisms-alternative morphs produced through plasticity-can reveal the evolutionary and ecological processes that initiate and maintain diversity within populations. We examined lifetime fitness consequences of two morphs in a polyphenic population of Arizona tiger salamanders using a 27-year data set with 1,317 adults and 6,862 captures across eight generations. Larval salamanders develop into either an aquatic paedomorph that retains larval traits and stays in its natal pond or a terrestrial metamorph that undergoes metamorphosis. To evaluate the adaptive significance of this polyphenism, we compared lifetime reproductive success of each morph and assessed how life-history strategies and spatiotemporal variation explained fitness. We found sex-specific differences in lifetime fitness between morphs. For males, paedomorphs had more reproductive opportunities than metamorphs when we accounted for the potential mating advantage of larger males. For females, in contrast, metamorphs had higher estimated egg production than paedomorphs. Life-history strategies differed between morphs largely because the morphs maximized different ends of the trade-off between age at first reproduction and longevity. Spatiotemporal variation affected larval more than adult life-history traits, with little to no effect on lifetime fitness. Thus, environmental variation likely explains differences in morph production across time and space but contributes little to lifetime fitness differences between morphs and sexes. Our long-term study and measures of lifetime fitness provide unique insight into the complex selective regimes potentially acting on each morph and sex. Our findings motivate future work to examine how sex-specific selection may contribute to the maintenance of polyphenism.

A mother's legacy: the strength of maternal effects in animal populations.

Although mothers influence the traits of their offspring in many ways beyond the transmission of genes, it remains unclear how important such 'maternal effects' are to phenotypic differences among individuals. Synthesizing estimates derived from detailed pedigrees, we evaluated the amount of phenotypic variation determined by maternal effects in animal populations. Maternal effects account for half as much phenotypic variation within populations as do additive genetic effects. Maternal effects most greatly affect morphology and phenology but, surprisingly, are not stronger in species with prolonged maternal care than in species without. While maternal effects influence juvenile traits more than adult traits on average, they do not decline across ontogeny for behaviour or physiology, and they do not weaken across the life cycle in species without maternal care. These findings underscore maternal effects as an important source of phenotypic variation and emphasise their potential to affect many ecological and evolutionary processes.

Modeling the population dynamics and community impacts of Ambystoma tigrinum: A case study of phenotype plasticity.

Phenotypic plasticity is the ability of an organism to change its phenotype in response to changes in the environment. General mathematical descriptions of the phenomenon rely on an abstract measure of "viability" that, in this study, is instantiated in the case of the Tiger Salamander, Ambystoma tigrinum. This organism has a point in its development when, upon maturing, it may take two very different forms. One is a terrestrial salamander (metamorph)that visits ponds to reproduce and eat, while the other is an aquatic form (paedomorph) that remains in the pond to breed and which consumes a variety of prey including its own offspring. A seven dimensional nonlinear system of ordinary differential equations is developed, incorporating small (Z) and large (B) invertebrates, Ambystoma young of the year (Y), juveniles (J), terrestrial metamorphs (A) and aquatic paedomorphs (P). One parameter in the model controls the proportion of juveniles maturing into A versus P. Solutions are shown to remain non-negative. Every effort was made to justify parameters biologically through studies reported in the literature. A sensitivity analysis and equilibrium analysis of model parameters demonstrate that morphological choice is critical to the overall composition of the Ambystoma population. Various population viability measures were used to select optimal percentages of juveniles maturing into metamorphs, with optimal choices differing considerably depending on the viability measure. The model suggests that the criteria for viability for this organism vary, both from location to location and also in time. Thus, optimal responses change with spatiotemporal variation, which is consistent with other phenotypically plastic systems. Two competing hypotheses for the conditions under which metamorphosis occurs are examined in light of the model and data from an Ambystoma tigrinum population at Mexican Cut, Colorado. The model clearly supports one of these over the other for this data set. There appears to be a mathematical basis to the general tenet of spatiotemporal variation being important for the maintenance of polyphenisms, and our results suggest that such variation may have cascading effects on population, community, and perhaps ecosystem dynamics because it drives the production of a keystone, cannibalistic predator.

Maternal investment mediates offspring life history variation with context-dependent fitness consequences.

Maternal effects, such as per capita maternal investment, often interact with environmental conditions to strongly affect traits expressed early in ontogeny. However, their impact on adult life history traits and fitness components is relatively unknown. Theory predicts that lower per capita maternal investment will have strong fitness costs when the offspring develop in unfavorable conditions, yet few studies have experimentally manipulated per capita maternal investment and followed offspring through adulthood. We used a surgical embryonic yolk removal technique to investigate how per capita maternal investment interacted with an important ecological factor, larval density, to mediate offspring life history traits through reproductive maturity in an amphibian, Ambystoma talpoideum. We predicted that increased larval density would reinforce the life history variation induced by differences in per capita investment (i.e., Controls vs. Reduced Yolk), with Reduced larvae ultimately expressing traits associated with lower fitness than Controls when raised at high densities. We found that Reduced individuals were initially smaller and more developed, caught up in size to Controls within the first month of the larval stage, but were smaller at the end of the larval stage in low densities. Reduced individuals also were more likely to undergo metamorphosis at high densities and mature 'females invested in more eggs for their body sizes than Controls. Together, our results do not support our hypothesis, but instead indicate that Reduced individuals express traits associated with higher fitness when they develop in high-density environments, but lower fitness in low-density environments. The observed life history and fitness patterns are consistent with the "maternal match" hypothesis, which predicts that when the maternal environment (e.g., high density) results in phenotypic variation that is transmitted to the offspring (e.g., reduced per capita yolk investment), and offspring face that same environment (e.g., high larval density), the fitness of both mother and offspring is maximized.

Non-additive effects of intra- and interspecific competition between two larval salamanders.

Assessment of the relative strengths of intra- and interspecific competition has increased in recent years and is critical to understanding the importance of competition. Yet, whether intra- and interspecific competition can have non-additive effects has rarely been tested. The resulting fitness consequences of such non-additive interactions are important to provide the context necessary to advance our understanding of competition theory. We compared the strength of additive and non-additive intra- and interspecific competition by manipulating densities of a pair of larval salamanders (Ambystoma talpoideum and A. maculatum) in experimental mesocosms within a response surface design. Intraspecific density had the strongest effect on the strength of competition for both species, and few observed comparisons indicated interspecific competition was an important factor in predicting body size, growth or larval period length of either species. Non-additive effects of intra- and interspecific competition influenced some response variables, including size and mass at metamorphosis in A. maculatum, but at a reduced strength compared to intraspecific effects alone. Intraspecific competition was thus the dominant biotic interaction, but non-additive effects also impact the outcome of competition in these species, validating the importance of testing for and incorporating non-additive density effects into competition models.

Consumptive and nonconsumptive effects of cannibalism in fluctuating age-structured populations.

Theory and empirical studies suggest that cannibalism in age-structured populations can regulate recruitment depending on the intensity of intraspecific competition between cannibals and victims and the nature of the cannibalism window, i.e., which size classes interact as cannibals and victims. Here we report on a series of experiments that quantify that window for age-structured populations of salamander larvae and paedomorphic adults. We determined body size limits on cannibalism in microcosms and then the consumptive and nonconsumptive (injuries, foraging and activity, diet, growth) effects on victims in mesocosms with seminatural levels of habitat complexity and alternative prey. We found that cannibalism by the largest size classes (paedomorphs and > or = age 3+ yr larvae) occurs mainly on young-of-the-year (YOY) victims. Surviving YOY and other small larvae had increased injuries, reduced activity levels, and reduced growth rates in the presence of cannibals. Data on YOY survival in an experiment in which we manipulated the density of paedomorphs combined with historical data on the number of cannibals in natural populations indicate that dominant cohorts of paedomorphs can cause observed recruitment failures. Dietary data indicate that ontogenetic shifts in diet should preclude strong intraspecific competition between YOY and cannibals in this species. Thus our results are consistent with previous empirical and theoretical work that suggests that recruitment regulation by cannibalism is most likely when YOY are vulnerable to cannibalism but have low dietary overlap with cannibals. Understanding the role of cannibalism in regulating recruitment in salamander populations is timely, given the widespread occurrences of amphibian decline. Previous studies have focused on extrinsic (including anthropogenic) factors that affect amphibian population dynamics, whereas the data presented here combined with long-term field observations suggest the potential for intrinsically driven population cycles.

Effects of pulsed nitrate exposure on amphibian development.

Most toxicity tests investigate constant concentrations of a chemical. Concentrations of many compounds in the environment are dynamic, however, and individuals may be more sensitive to pulses of a chemical initiated at specific points during development. Realistic toxicity tests are important to accurately assess the toxicity of a compound. Bufo americanus and Hyla chrysoscelis tadpoles were exposed to concentrations of nitrate, a pervasive stressor in the environment, up to 5 mg/L of NO3-N in constant concentrations and in pulses at three different points during development. At the termination of the experiments, individuals were measured for developmental stability (DS) and traditional fitness correlates (size, body condition, and time to metamorphosis). No significant differences were found in these measures between treatments and controls in B. americanus tadpoles. In H. chrysoscelis, however, more extreme directional asymmetry was found in the middle and late pulses, indicating that the sudden change in concentration of nitrate decreased the level of DS in tadpoles. These results indicate that nitrate has subtle but important effects at low doses, and they suggest that species may be better able to deal with pulses that occur early rather than late in development. A greater understanding about the effects of pulses will help conservation biologists to manage populations and prevent population declines.

Effects of nitrate on embryos of three amphibian species.

Embryos of three aquatic breeding amphibian species, Ambystoma mexicanum, Hyla chrysoscelis, and Rana clamitans, were exposed to increasing levels (0, 5, 10, 30, 60, 100, 300, and 500 mg/L) of nitrate-N (NO(3)-) in laboratory, static-renewal experiments. Lethal effects were recorded from Gosner stage 2 (H. chrysoscelis and R. clamitans) or Harrison stage 2 (A. mexicanum) to time of hatching. Date of hatching and length at hatching were also compared between treatments for A. mexicanum. No significant differences in mortality between treatments were found between the three species. A. mexicanum in the 300 and 500 mg/L treatments hatched significantly earlier than individuals in the other treatment groups and, consequently, were significantly shorter in length at hatching. However, no effect on length was detected when days until hatching was considered as a covariate in the analysis. This study supports other recent research showing little to no effect of NO(3)- on amphibian embryos. The lack of effect at such high nitrate concentrations raises questions about the specific mechanisms responsible for protecting amphibians from NO(3)- during embryonic development, especially when compared to other chemicals that have shown more deleterious effects.

Paedomorphosis in Ambystoma talpoideum: 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.

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.

SEXUAL SELECTION IN AMERICAN TOADS: A TEST OF A GOOD-GENES HYPOTHESIS.

Adaptive mate choice in species lacking male resource control and/or paternal care might be maintained by selection because preferred males sire genetically superior offspring. For such a process to occur, some male phenotypic trait(s) must both reliably indicate male genetic quality and influence the pattern of mate choice by females. In American toads, Bufo americanus, male body length has been documented to influence female mating patterns: females usually mate with males that are larger than average. However, the relationship between male size and male genetic quality is unknown. We conducted a controlled breeding experiment using 48 sires and 19 dams to determine if larger males sire offspring with superior larval performance characteristics (greater survival to metamorphosis, larger mass at metamorphosis, and earlier metamorphosis). We also aged each sire to test the hypothesis that older males are, on average, genetically superior to younger males. We crossed each female with three sires representing three body size categories (mean and 1 SD ± mean snout-ischium length). Hatchlings (500 from each cross) were reared to metamorphosis in seminatural ponds in the field. Metamorph weight (log transformed) and age at metamorphosis showed significant heritability and were genetically correlated with each other. Hence, sires differed in genetic quality. However, none of the three measures of offspring performance was correlated with sire body size or age. Thus, we obtained no support for the prediction that sire body size or age is related to genetic quality.