skip to main content
US FlagAn official website of the United States government
dot gov icon
Official websites use .gov
A .gov website belongs to an official government organization in the United States.
https lock icon
Secure .gov websites use HTTPS
A lock ( lock ) or https:// means you've safely connected to the .gov website. Share sensitive information only on official, secure websites.


Title: Polyphenism predicts actuarial senescence and lifespan in tiger salamanders
Abstract 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.  more » « less
Award ID(s):
2153273
PAR ID:
10498645
Author(s) / Creator(s):
; ; ; ;
Publisher / Repository:
British Ecological Society
Date Published:
Journal Name:
Journal of Animal Ecology
Volume:
93
Issue:
3
ISSN:
0021-8790
Page Range / eLocation ID:
333 to 347
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Colchero, Fernando (Ed.)
    Abstract Differences among individuals within a population are ubiquitous. Those differences are known to affect the entire life cycle with important consequences for all demographic rates and outcomes. One source of among‐individual phenotypic variation that has received little attention from a demographic perspective is animal personality, which is defined as consistent and heritable behavioural differences between individuals. While many studies have shown that individual variation in individual personality can generate individual differences in survival and reproductive rates, the impact of personality on all demographic rates and outcomes remains to be assessed empirically.Here, we used a unique, long‐term, dataset coupling demography and personality of wandering albatross (Diomedea exulans) in the Crozet Archipelago and a comprehensive analysis based on a suite of approaches (capture‐mark‐recapture statistical models, Markov chains models and structured matrix population models). We assessed the effect of boldness on annual demographic rates (survival, breeding probability, breeding success), life‐history outcomes (life expectancy, lifetime reproductive outcome, occupancy times), and an integrative demographic outcome (population growth rate).We found that boldness had little impact on female demographic rates, but was very likely associated with lower breeding probabilities in males. By integrating the effects of boldness over the entire life cycle, we found that bolder males had slightly lower lifetime reproductive success compared to shyer males. Indeed, bolder males spent a greater proportion of their lifetime as non‐breeders, which suggests longer inter‐breeding intervals due to higher reproductive allocation.Our results reveal that the link between boldness and demography is more complex than anticipated by the pace‐of‐life literature and highlight the importance of considering the entire life cycle with a comprehensive approach when assessing the role of personality on individual performance and demography. 
    more » « less
  2. Abstract Polyphenisms occur when phenotypic plasticity produces morphologically distinct phenotypes from the same genotype. Plasticity is maintained through fitness trade‐offs which are conferred to different phenotypes under specific environmental contexts. Predicting the impacts of contemporary climate change on phenotypic plasticity is critical for climate‐sensitive animals like amphibians, but elucidating the selective pressures maintaining polyphenisms requires a framework to control for all mechanistic drivers of plasticity.Using a 32‐year dataset documenting the larval and adult histories of 717 Arizona tiger salamanders (Ambystoma mavortium nebulosum), we determined how annual variation in climate and density dependence explained the maintenance of two distinct morphs (terrestrial metamorph vs. aquatic paedomorph) in a high‐elevation polyphenism. The effects of climate and conspecific density on morph development were evaluated with piecewise structural equation models (SEM) to tease apart the direct and indirect pathways by which these two mechanisms affect phenotypic plasticity.Climate had a direct effect on morph outcome whereby longer growing seasons favoured metamorphic outcomes. Also, climate had indirect effects on morph outcome as mediated through density‐dependent effects, such as long overwintering coldspells corresponding to high cannibal densities and light snowpacks corresponding to high larval densities, both of which promoted paedomorphic outcomes.Both climate and density dependence serve as important proxies for growth and resource limitation, which are important underlying drivers of the phenotypic plasticity in animal polyphenisms. Our findings motivate new studies to determine how contemporary climate change will alter the selective pressures maintaining phenotypic plasticity and polyphenisms. 
    more » « less
  3. Abstract Maternal age can influence reproductive success and offspring fitness, but the timing, magnitude and direction of those impacts are not well understood. Evolutionary theory predicts that selection on fertility senescence is stronger than maternal effect senescence, and therefore, the rate of maternal effect senescence will be faster than fertility senescence.We used a 36‐year study of northern elephant seals (Mirounga angustirostris) to investigate reproductive senescence. Our dataset included 103,746 sightings of 1203 known‐age female northern elephant seals.We hypothesized that fertility (maternal reproductive success), offspring survival and recruitment into the breeding population, and male offspring production would decline with advanced maternal age. Furthermore, we hypothesized that older females would shorten their moulting haul out to allow for more time spent foraging.We found evidence for both fertility and maternal effect senescence, but no evidence for senescence impacting offspring recruitment or sex ratio. Breeding probability declined from 96.4% (95% CI: 94.8%–97.5%) at 11 years old to 89.7% (81.9%–94.3%) at 19 years old, and the probability of offspring survival declined from 30.3% (23.6%–38.0%) at 11 years old to 9.1% (3.2%–22.9%) at 19 years old.The rates of decline for fertility and maternal effect senescence were not different from each other. However, maternal effect senescence had a substantially greater impact on the number of offspring surviving to age 1 compared to fertility senescence. Compared to a hypothetical non‐senescent population, maternal effect senescence resulted in 5.3% fewer surviving pups, whereas fertility senescence resulted in only 0.3% fewer pups produced per year. These results are consistent with evolutionary theory predicting weaker selection on maternal effect than fertility senescence. Maternal effect senescence may therefore be more influential on population dynamics than fertility senescence in some systems. 
    more » « less
  4. Abstract Sex‐related differences in vital rates that drive population change reflect the basic life history of a species. However, for visually monomorphic bird species, determining the effect of sex on demographics can be a challenge. In this study, we investigated the effect of sex on apparent survival, recruitment, and breeding propensity in the Adélie penguin (Pygoscelis adeliae), a monochromatic, slightly size dimorphic species with known age, known sex, and known breeding history data collected during 1996–2019 (n = 2127 birds) from three breeding colonies on Ross Island, Antarctica. Using a multistate capture–mark–recapture maximum‐likelihood model, we estimated apparent survival (), recapture (resighting) probability (), and the probability of transitioning among breeding states and moving between colonies (; colony‐specific non‐juvenile pre‐breeders, breeders, and non‐breeders). Survival rate varied by breeding status and colony, but not sex, and pre‐breeders had higher survival rates than breeders and non‐breeders. Females had a higher probability of recruiting into the breeding population each year and may enter the breeding pool at younger ages. In contrast, both sexes had the same probability of breeding from year to year once they had recruited. Although we detected no direct sex effects on survival, the variation in recruitment probability and age‐at‐first reproduction, along with lower survival rates of breeders compared to pre‐breeders, likely leads to shorter lifespans for females. This is supported by our findings of a male‐biased mean adult sex ratio (ASR) of 1.4 males for every female ( proportion of males = 0.57, SD = 0.07) across all colonies and years in this metapopulation. Our study illustrates how important it can be to disentangle sex‐related variation in population vital rates, particularly for species with complex life histories and demographic dynamics. 
    more » « less
  5. Alison Davis Rabosky (Ed.)
    Abstract 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. 
    more » « less