An official website of the United States government
Identifying the mechanisms underlying the persistence of rare species has long been a motivating question for ecologists. Classical theory implies that community dynamics should be driven by common species, and that natural selection should not allow small populations of rare species to persist. Yet, a majority of the species found on Earth are rare. Consequently, several mechanisms have been proposed to explain their persistence, including negative density dependence, demographic compensation, vital rate buffering, asynchronous responses of subpopulations to environmental heterogeneity, and fine‐scale source‐sink dynamics. Persistence of seeds in a seed bank, which is often ignored in models of population dynamics, can also buffer small populations against collapse. We used integral projection models (IPMs) to examine the population dynamics ofOenothera coloradensis, a rare, monocarpic perennial forb, and determine whether any of five proposed demographic mechanisms for rare species persistence contribute to the long‐term viability of two populations. We also evaluate how including a discrete seed bank stage changes these population models. Including a seed bank stage in population models had a significantly increased modeledO. coloradensispopulation growth rate. Using this structured population model, we found that negative density‐dependence was the only supported mechanism for the persistence of this rare species. We propose that high micro‐site abundances within a spatially heterogeneous environment enables this species to persist, allowing it to sidestep the demographic and genetic challenges of small population size that rare species typically face. The five mechanisms of persistence explored in our study have been demonstrated as effective strategies in other species, and the fact that only one of them had strong support here supports the idea that globally rare species can employ distinct persistence strategies. This reinforces the need for customized management and conservation strategies that mirror the diversity of mechanisms that allow rare species persistence.
more »
« less
How differing modes of non‐genetic inheritance affect population viability in fluctuating environments
Abstract Different modes of non‐genetic inheritance are expected to affect population persistence in fluctuating environments. We here analyseCaenorhabditis elegansdensity‐independent per capita growth rate time series on 36 populations experiencing six controlled sequences of challenging oxygen level fluctuations across 60 generations, and parameterise competing models of non‐genetic inheritance in order to explain observed dynamics. Our analysis shows that phenotypic plasticity and anticipatory maternal effects are sufficient to explain growth rate dynamics, but that a carryover model where ‘epigenetic’ memory is imperfectly transmitted and might be reset at each generation is a better fit to the data. We further find that this epigenetic memory is asymmetric since it is kept for longer when populations are exposed to the more challenging environment. Our analysis suggests that population persistence in fluctuating environments depends on the non‐genetic inheritance of phenotypes whose expression is regulated across multiple generations.
more »
« less
- Award ID(s):
- 1725797
- PAR ID:
- 10459707
- Publisher / Repository:
- Wiley-Blackwell
- Date Published:
- Journal Name:
- Ecology Letters
- Volume:
- 22
- Issue:
- 11
- ISSN:
- 1461-023X
- Page Range / eLocation ID:
- p. 1767-1775
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Pagliara, Stefano (Ed.)ABSTRACT Non-genetic factors can cause significant fluctuations in gene expression levels. Regardless of growing in a stable environment, this fluctuation leads to cell-to-cell variability in an isogenic population. This phenotypic heterogeneity allows a tiny subset of bacterial cells in a population called persister cells to tolerate long-term lethal antibiotic effects by entering into a non-dividing, metabolically repressed state. We occasionally noticed a high variation in persister levels, and to explore this, we tested clonal populations starting from a single cell using a modified Luria-Delbrück fluctuation test. Although we kept the conditions same, the diversity in persistence level among clones was relatively consistent: varying from ~60- to 100- and ~40- to 70-fold for ampicillin and apramycin, respectively. Then, we divided and diluted each clone to observe whether the same clone had comparable persister levels for more than one generation. Replicates had similar persister levels even when clones were divided, diluted by 1:20, and allowed to grow for approximately five generations. This result explicitly shows a cellular memory passed on for generations and eventually lost when cells are diluted to 1:100 and regrown (>seven generations). Our result demonstrates (1) the existence of a small population prepared for stress (“primed cells”) resulting in higher persister numbers; (2) the primed memory state is reproducible and transient, passed down for generations but eventually lost; and (3) a heterogeneous persister population is a result of a transiently primed reversible cell state and not due to a pre-existing genetic mutation. IMPORTANCEAntibiotics have been highly effective in treating lethal infectious diseases for almost a century. However, the increasing threat of antibiotic resistance is again causing these diseases to become life-threatening. The longer a bacteria can survive antibiotics, the more likely it is to develop resistance. Complicating matters is that non-genetic factors can allow bacterial cells with identical DNA to gain transient resistance (also known as persistence). Here, we show that a small fraction of the bacterial population called primed cells can pass down non-genetic information (“memory”) to their offspring, enabling them to survive lethal antibiotics for a long time. However, this memory is eventually lost. These results demonstrate how bacteria can leverage differences among genetically identical cells formed through non-genetic factors to form primed cells with a selective advantage to survive antibiotics.more » « less
-
Environmental factors can promote phenotypic variation through alterations in the epigenome and facilitate adaptation of an organism to the environment. Although hydrogen sulfide is toxic to most organisms, the fish Poecilia mexicana has adapted to survive in environments with high levels that exceed toxicity thresholds by orders of magnitude. Epigenetic changes in response to this environmental stressor were examined by assessing DNA methylation alterations in red blood cells, which are nucleated in fish. Males and females were sampled from sulfidic and nonsulfidic natural environments; individuals were also propagated for two generations in a nonsulfidic laboratory environment. We compared epimutations between the sexes as well as field and laboratory populations. For both the wild-caught (F0) and the laboratory-reared (F2) fish, comparing the sulfidic and nonsulfidic populations revealed evidence for significant differential DNA methylation regions (DMRs). More importantly, there was over 80% overlap in DMRs across generations, suggesting that the DMRs have stable generational inheritance in the absence of the sulfidic environment. This is an example of epigenetic generational stability after the removal of an environmental stressor. The DMR-associated genes were related to sulfur toxicity and metabolic processes. These findings suggest that adaptation of P. mexicana to sulfidic environments in southern Mexico may, in part, be promoted through epigenetic DNA methylation alterations that become stable and are inherited by subsequent generations independent of the environment.more » « less
-
Evolutionary feedbacks occur when evolution in one generation alters the environment experienced by subsequent generations and are an expected result of indirect genetic effects (IGEs). Hypotheses abound for the role of evolutionary feedbacks in climate change, agriculture, community dynamics, population persistence, social interactions, the genetic basis of evolution, and more, but evolutionary feedbacks have rarely been directly measured experimentally, leaving open questions about how feedbacks influence evolution. Using experimental evolution, we manipulated the social environment in which aggression was expressed and selected in fruit fly (Drosophila melanogaster) populations to allow or limit feedbacks. We selected for increased male–male aggression while allowing either positive, negative, or no feedbacks, alongside unselected controls. We show that populations undergoing negative feedbacks had the weakest evolutionary changes in aggression, while populations undergoing positive evolutionary feedbacks evolved supernormal aggression. Further, the underlying social dynamics evolved only in the negative feedbacks treatment. Our results demonstrate that IGE-mediated evolutionary feedbacks can alter the rate and pattern of behavioral evolution.more » « less
-
Abstract Organisms are experiencing higher average temperatures and greater temperature variability because of anthropogenic climate change. Some populations respond to changes in temperature by shifting their ranges or adjusting their phenotypes via plasticity and/or evolution, while others go extinct. Predicting how populations will respond to temperature changes is challenging because extreme and unpredictable climate changes will exert novel selective pressures. For this reason, there is a need to understand the physiological mechanisms that regulate organismal responses to temperature changes. In vertebrates, glucocorticoid hormones mediate physiological and behavioral responses to environmental stressors and thus are likely to play an important role in how vertebrates respond to global temperature changes. Glucocorticoids have cascading effects that influence the phenotype and fitness of individuals, and some of these effects can be transmitted to offspring via trans- or intergenerational effects. Consequently, glucocorticoid-mediated responses could affect populations and could even be a powerful driver of rapid evolutionary change. Here, we present a conceptual framework that outlines how temperature changes due to global climate change could affect population persistence via glucocorticoid responses within and across generations (via epigenetic modifications). We briefly review glucocorticoid physiology, the interactions between environmental temperatures and glucocorticoid responses, and the phenotypic consequences of glucocorticoid responses within and across generations. We then discuss possible hypotheses for how glucocorticoid-mediated phenotypic effects might impact fitness and population persistence via evolutionary change. Finally, we pose pressing questions to guide future research. Understanding the physiological mechanisms that underpin the responses of vertebrates to elevated temperatures will help predict population-level responses to the changing climates we are experiencing.more » « less
