An official website of the United States government
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
Plastic mechanisms for unraveling a universal trade-off between water loss and respiration
Abstract Phenotypic expression is often constrained by functional conflicts between traits, and the resulting trade-offs impose limits on phenotypic and taxonomic diversity. However, the underlying mechanisms that maintain trade-offs or allow organisms to resolve them via phenotypic plasticity are often challenging to detect. The trade-off between gas exchange and water loss across respiratory surfaces represents a fundamental trade-off that constrains phenotypic diversity in terrestrial life. Here, we investigate plastic mechanisms that mitigate this trade-off in lungless salamanders that breathe exclusively across their skin. Our field and laboratory experiments identified plastic responses to environmental variation in water loss and oxygen uptake, and gene expression analyses identified putative pathways that regulate this trade-off. Although the trade-off was generally strong, its strength covaried with environmental conditions. At the molecular level, antagonistic pleiotropy in multiple biological pathways (e.g., vasoconstriction and upregulation of aerobic respiration) putatively produce the trade-off, while other pathways mitigate the trade-off by affecting a single trait (e.g., oxygen binding affinity, melanin synthesis). However, organisms are likely to encounter novel trade-offs in the process of bypassing another. Our study provides evidence that alternative pathways allow organisms to mitigate pleiotropic conflicts, which ultimately may allow greater phenotypic diversity and persistence in novel environments.
more »
« less
- Award ID(s):
- 2401987
- PAR ID:
- 10600649
- Publisher / Repository:
- Oxford University Press
- Date Published:
- Journal Name:
- Evolution
- Volume:
- 79
- Issue:
- 6
- ISSN:
- 0014-3820
- Format(s):
- Medium: X Size: p. 1073-1085
- Size(s):
- p. 1073-1085
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Synopsis In response to rapidly changing environmental conditions, many organisms are experiencing shifts in geographic ranges and in the timing and expression of key life-history traits, which have important effects on fitness. However, the physiological mechanisms that mediate these phenotypic responses, such as endocrine and other signaling pathways are not well understood. This information will be critical for predicting organismal responses to climate change because physiological mechanisms are often highly responsive to environmental cues and influence the phenotypic variation available to selection. Additionally, they often integrate suites of correlated traits and are thus expected to influence the evolutionary response to selection. The overarching goals of this symposium were to gain novel insights into the physiological mechanisms that underlie organismal responses to rapidly changing environmental conditions and to identify gaps in knowledge and experimental approaches to advance the field. Here we review and discuss the symposium contributions and the research themes that emerged as important foci for future studies.more » « less
-
Fluctuating environmental conditions are ubiquitous in natural systems, and populations have evolved various strategies to cope with such fluctuations. The particular mechanisms that evolve profoundly influence subsequent evolutionary dynamics. One such mechanism is phenotypic plasticity, which is the ability of a single genotype to produce alternate phenotypes in an environmentally dependent context. Here, we use digital organisms (self-replicating computer programs) to investigate how adaptive phenotypic plasticity alters evolutionary dynamics and influences evolutionary outcomes in cyclically changing environments. Specifically, we examined the evolutionary histories of both plastic populations and non-plastic populations to ask: (1) Does adaptive plasticity promote or constrain evolutionary change? (2) Are plastic populations better able to evolve and then maintain novel traits? And (3), how does adaptive plasticity affect the potential for maladaptive alleles to accumulate in evolving genomes? We find that populations with adaptive phenotypic plasticity undergo less evolutionary change than non-plastic populations, which must rely on genetic variation from de novo mutations to continuously readapt to environmental fluctuations. Indeed, the non-plastic populations undergo more frequent selective sweeps and accumulate many more genetic changes. We find that the repeated selective sweeps in non-plastic populations drive the loss of beneficial traits and accumulation of maladaptive alleles, whereas phenotypic plasticity can stabilize populations against environmental fluctuations. This stabilization allows plastic populations to more easily retain novel adaptive traits than their non-plastic counterparts. In general, the evolution of adaptive phenotypic plasticity shifted evolutionary dynamics to be more similar to that of populations evolving in a static environment than to non-plastic populations evolving in an identical fluctuating environment. All natural environments subject populations to some form of change; our findings suggest that the stabilizing effect of phenotypic plasticity plays an important role in subsequent adaptive evolution.more » « less
-
ABSTRACT Evolutionary responses to climate change may incur trade‐offs due to energetic constraints and mechanistic limitations, which are both influenced by environmental context. Adaptation to one stressor may result in life history trade‐offs, canalization of phenotypic plasticity, and the inability to tolerate other stressors, among other potential costs. While trade‐offs incurred during adaptation are difficult to detect in natural populations, experimental evolution can provide important insights by measuring correlated responses to selection as populations adapt to changing environments. However, studies testing for trade‐offs have generally lagged behind the growth in the use of experimental evolution in climate change studies. We argue that the important insights generated by the few studies that have tested for trade‐offs make a strong case for including these types of measurements in future studies of climate adaptation. For example, there is emerging consensus from experimental evolution studies that tolerance and tolerance plasticity trade‐offs are an often‐observed outcome of adaptation to anthropogenic change. In recent years, these types of studies have been strengthened by the use of sequencing of experimental populations, which provides promising new avenues for understanding the molecular mechanisms underlying observed phenotypic trade‐offs.more » « less
-
Synopsis The concept of trade-offs permeates our thinking about adaptive evolution because they are exhibited at every level of biological organization, from molecular and cellular processes to organismal and ecological functions. Trade-offs inevitably arise because different traits do not occur in isolation, but instead are imbedded within complex, integrated systems that make up whole organisms. The genetic and mechanistic underpinning of trade-offs can be found in the pleiotropic nodes that occur in the biological pathways shared between traits. Yet, often trade-offs are only understood as statistical correlations, limiting the ability to evaluate the interplay between how selection and constraint interact during adaptive evolution. Here, we first review the classic paradigms in which physiologists and evolutionary biologists have studied trade-offs and highlight the ways in which network and molecular pathway approaches unify these paradigms. We discuss how these approaches allow researchers to evaluate why trade-offs arise and how selection can act to overcome trait correlations and evolutionary constraints. We argue that understanding how the conserved molecular pathways are shared between different traits and functions provides a conceptual framework for evolutionary biologists, physiologists, and molecular biologists to meaningfully work together toward the goal of understanding why correlations and trade-offs occur between traits. We briefly highlight the melanocortin system and the hormonal control of osmoregulation as two case studies where an understanding of shared molecular pathways reveals why trade-offs occur between seemingly unrelated traits. While we recognize that applying such approaches poses challenges and limitations particularly in the context of natural populations, we advocate for the view that focusing on the biological pathways responsible for trade-offs provides a unified conceptual context accessible to a broad range of integrative biologists.more » « less
