An official website of the United States government
Abstract Phenotypic plasticity is a strategy by which animals alter behaviour, morphology and/or physiology in response to cues of current conditions to cope with environmental heterogeneity.If environmental change is impending and cues reliably predict future conditions, animals can also respond in anticipation of these changes (i.e. anticipatory plasticity) if they possess the mechanistic architecture necessary to do so. This phenomenon has been documented across the tree of life, but how animals integrate cues of future conditions and mount anticipatory responses remains largely ambiguous.Here, we synthesize theoretical principles from sensory biology and animal communication with recent advances in physiological ecology to identify candidate physiological mechanisms underpinning anticipatory plasticity in animal systems.We discuss how socio‐ecological rhythms, cue perception and interactions between the epigenome, neuroendocrine system and gut microbiota can contribute to the maintenance and evolution of anticipatory plasticity, including anticipatory reproduction.We shed light on the proximate and ultimate mechanisms that facilitate the evolution and maintenance of anticipatory plasticity in the face of environmental heterogeneity, contributing to a broader understanding of how animals may respond to rapid global change as environmental cues become unreliable and conditions unpredictable. Read the freePlain Language Summaryfor this article on the Journal blog.
more »
« less
Decoupling the effects of food and density on life‐history plasticity of wild animals using field experiments: Insights from the steward who sits in the shadow of its tail, the North American red squirrel
Abstract Long‐term studies of wild animals provide the opportunity to investigate how phenotypic plasticity is used to cope with environmental fluctuations and how the relationships between phenotypes and fitness can be dependent upon the ecological context.Many previous studies have only investigated life‐history plasticity in response to changes in temperature, yet wild animals often experience multiple environmental fluctuations simultaneously. This requires field experiments to decouple which ecological factor induces plasticity in fitness‐relevant traits to better understand their population‐level responses to those environmental fluctuations.For the past 32 years, we have conducted a long‐term integrative study of individually marked North American red squirrelsTamiasciurus hudsonicusErxleben in the Yukon, Canada. We have used multi‐year field experiments to examine the physiological and life‐history responses of individual red squirrels to fluctuations in food abundance and conspecific density.Our long‐term observational study and field experiments show that squirrels can anticipate increases in food availability and density, thereby decoupling the usual pattern where animals respond to, rather than anticipate, an ecological change.As in many other study systems, ecological factors that can induce plasticity (such as food and density) covary. However, our field experiments that manipulate food availability and social cues of density (frequency of territorial vocalizations) indicate that increases in social (acoustic) cues of density in the absence of additional food can induce similar life‐history plasticity, as does experimental food supplementation.Changes in the levels of metabolic hormones (glucocorticoids) in response to variation in food and density are one mechanism that seems to induce this adaptive life‐history plasticity.Although we have not yet investigated the energetic response of squirrels to elevated density or its association with life‐history plasticity, energetics research in red squirrels has overturned several standard pillars of knowledge in physiological ecology.We show how a tractable model species combined with integrative studies can reveal how animals cope with resource fluctuations through life‐history plasticity.
more »
« less
- Award ID(s):
- 1749627
- PAR ID:
- 10455906
- Publisher / Repository:
- Wiley-Blackwell
- Date Published:
- Journal Name:
- Journal of Animal Ecology
- Volume:
- 89
- Issue:
- 11
- ISSN:
- 0021-8790
- Format(s):
- Medium: X Size: p. 2397-2414
- Size(s):
- p. 2397-2414
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Abstract Much research has shown that environmental stress can induce adaptive and maladaptive phenotypic changes in organisms that persist for multiple generations. Such transgenerational phenotypic plasticity shrouds our understanding of the long‐term consequences of ongoing anthropogenic pressures.Here, we evaluated within‐ and transgenerational phenotypic responses to food stress in the freshwater crustacean,Daphnia. We reared 45 clones ofDaphnia pulicariaeach on high‐qualityScenedesmusand low‐quality (but also non‐toxic) cyanobacteria (generation 1). Offspring produced by generation 1 adults were then reared onScenedesmus(generation 2), and life‐history traits were measured across both generations.The results show thatDaphniain generation 1 exhibited reduced fitness (i.e., delayed maturation, lower reproductive output, increased clutch interval) when reared in the presence of cyanobacteria as opposed to high‐quality food. However, maternal stress had no clear influence on the fitness of offspring. That is,Daphniain the second experimental generation had similar mean trait values, irrespective of whether their mothers were reared on cyanobacteria or high‐quality food.Signals of transgenerational life‐history effects were obscured, in part, by extensive clonal variation amongDaphniain the direction of transgenerational responses to cyanobacteria (i.e., adaptive and maladaptive plasticity). Further analyses demonstrated that such individual variance in plasticity might be open to selection and potentially offer a means of contemporary adaptation to cyanobacteria. Taken together, our results denote a link between the overall strength of transgenerational responses to the environment and the potential for rapid evolution in populations. A freePlain Language Summarycan be found within the Supporting Information of this article.more » « less
-
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
-
Abstract To cope with uncertainty and variability in their environment, plants evolve distinct life‐history strategies by allocating different fractions of energy to growth, survival and fecundity. These differences in life‐history strategies could potentially influence ecosystem‐level dynamics, such as the sensitivity of primary production to resource fluctuations. However, linkages between evolutionary and ecosystem dynamics are not well understood.We used an annual plant population model to ask, when might differences in plant life‐history strategies produce differences in the sensitivity of primary production to resource fluctuations?Consistent with existing theory, we found that a highly variable and unpredictable environment led to the evolution of a conservative strategy characterized by relatively low and invariant germination fractions, while a variable but predictable environment favoured a riskier strategy featuring more variable germination fractions. Unexpectedly, we found that the influence of life‐history strategy on the sensitivity of production to resource fluctuations depended on competitive interactions, specifically the rate at which production saturates with the number of competing individuals. Rapid saturation overwhelms the influence of life‐history strategy, but when production saturates more slowly, the risky strategy translated to high sensitivity, whereas the conservative strategy translated to low sensitivity.Empirical estimates from Sonoran Desert annual plant populations indicate that production saturates relatively rapidly with the number of individuals for most species, suggesting that life‐history differences are unlikely to alter sensitivity of production to resource fluctuations, at least in this community.Synthesis. Our modelling results imply that research to understand the sensitivity of primary production to resource fluctuations should focus more on the intraspecific competitive interactions shaping the density–yield relationship than on the life‐history strategies that determine temporal risk‐spreading.more » « less
-
Abstract Mathematical models highlighted the importance of pathogen‐mediated invasion, with the replacement of red squirrels by squirrelpox virus (SQPV) carrying grey squirrels in the UK, a well‐known example.In this study, we combine new epidemiological models, with a range of infection characteristics, with recent longitudinal field and experimental studies on the SQPV dynamics in red and grey squirrel populations to better infer the mechanistic basis of the disease interaction.A key finding is that a model with either partial immunity or waning immunity and reinfection, where individuals become seropositive on the second exposure to infection, that up to now has been shown in experimental data only, can capture the key aspects of the field study observations.By fitting to SQPV epidemic observations in isolated red squirrel populations, we can infer that SQPV transmission between red squirrels is significantly (4×) higher than the transmission between grey squirrels and as a result our model shows that disease‐mediated replacement of red squirrels by greys is considerably more rapid than replacement in the absence of SQPV.Our findings recover the key results of the previous model studies, which highlights the value of simple strategic models that are appropriate when there are limited data, but also emphasise the likely complexity of immune interactions in wildlife disease and how models can help infer disease processes from field data.more » « less
