Can individual variation in phenotypic plasticity enhance population viability?
Introduction
Individuals within a population may adjust behavioral, morphological or physiological responses to varying environmental conditions through phenotypic plasticity (Charmantier et al., 2008). Phenotypic plasticity, the ability of a genotype (i.e., an individual) to express different phenotypes as a function of the environmental conditions being experienced (Bradshaw, 1965, Pigliucci, 2001), is a widely documented phenomenon in natural populations (Gotthard and Nylin, 1995). Plasticity can influence vital rates, and thereby population dynamics and extinction risk. As a result, phenotypic plasticity is potentially a key element that allows populations to respond non-genetically to environmental change and variability (Chevin et al., 2010, Reed et al., 2010, Stearns, 1989, Visser, 2008). Given that climate change can alter the environmental conditions experienced by many organisms, it is important to explore the population-level consequences of individual phenotypic plasticity since change in environmental conditions can affect the availability of resources, with consequences for the energy available to an organism and thereby its fitness.
Seasonal environments create challenges for organisms with regard to annual biological events, such as the timing of reproduction, especially when environmental factors vary from one year to the next (Reed et al., 2010). Organisms may undergo behavioral, physiological and morphological responses as a way to cope with seasonal variation in food resource. During winter, organisms may undergo a period of reduced energy intake that results in a depletion of energy reserves and body mass, whereas during the summer organisms build energy reserves and increase their body mass. Moreover, an individual’s body condition at the end of the winter period may influence fitness in the following season (Harrison et al., 2011). Body mass dynamics are, therefore, a key element that can affect life-history processes of a species, including survival and reproduction (Blanckenhorn, 2000). Thus, we might expect natural selection to favor response mechanisms that permit individuals to compensate for an environmentally induced period of slow growth (Metcalfe and Monaghan, 2003).
In seasonal environments, individuals can cope with the consequences of a harsh period such as winter through compensatory growth (Nicieza and Metcalfe, 1997, De Block et al., 2007). Compensatory growth is a form of phenotypic plasticity (Ab Ghani and Merilä, 2014) by which individuals respond to environmental cues indicating that an individual is relatively small at a given point in time with regard to future energy needs (Metcalfe and Monaghan, 2001). Compensatory growth allows individuals to compensate by accelerating growth rates to reduce the risk of having a sub-optimal size during a future stressful period (Ali et al., 2003, Metcalfe and Monaghan, 2001). Compensation may occur in structural components as well as body mass (Abrams et al., 1996, Metcalfe and Monaghan, 2001, Nicieza and Metcalfe, 1997) and, in both cases, influence an individual’s fitness (Blanckenhorn, 2000, Stearns, 1992). The fact that growth rates vary among individuals within a population (Kvist and Lindström, 2001), suggests that there may be plasticity in growth rates among individuals due to differences in body mass since growth rates respond to the individual’s current body condition or state (Hornick et al., 2000, Metcalfe and Monaghan, 2001). Compensatory growth may, however, be costly (reviewed in Dmitriew, 2011, Hector and Nakagawa, 2012). Depending on whether accelerated growth affects energy allocation, individuals that accelerate their growth rate through increased foraging may pay an immediate cost in the form of delays in structural development (Arendt and Wilson, 2000), individual performance (e.g. swimming sprinting speed; Killen et al., 2014)reduced investment in tissue maintenance (Morgan et al., 2000) or reproduction (Auer et al., 2010, Lee et al., 2012, Lee et al., 2016), increased risk of predation while foraging (Gotthard, 2000). Rapid growth may lead to longer-term costs when it results in damage at the physiological or cellular level (Jennings et al., 1999; and reviewed in Metcalfe and Monaghan, 2001, Metcalfe and Monaghan, 2003) and on a decreased lifespan (Lee et al., 2013). Furthermore, other costs, such as reduced quality and fitness of offspring, can also be expected, but these have been less well explored (Ab Ghani and Merilä, 2014).
Here, we develop a non-spatially explicit individual-based model (IBM) to study the effects of phenotypically plastic responses of seasonal growth rate (herein compensatory growth) on the probability of population extinction. In our model, individuals can respond, in general, to the changes in environmental conditions through phenotypic plasticity, paying an immediate cost when they do so. The cost paid by individuals was assumed to be less than the benefits gained through plasticity. Additionally, we assumed that individuals may differ in their degree of plastic response to environmental conditions. Thus, we hypothesize that if individuals start the foraging season in poor conditions (i.e., they are below the average June body mass), then they can compensate by gaining mass faster than would occur absent a plastic response, whereas individuals in good condition will put on mass without responding plastically. This compensatory response can reduce the probability of extinction of a population under more extreme climate scenarios.
Our model focuses on the population dynamics of a well-studied population of yellow-bellied marmots, Marmota flaviventris; obligately hibernating, ground dwelling, sciurid rodents, in Colorado (Armitage, 2014, Blumstein, 2013). Marmots at this location have increased their end-of-season body mass over the past 12 years, which means that they now enter hibernation in better body condition and have reduced over-winter mortality (Ozgul et al., 2010). Ozgul et al. (2010) suggested that the increase in body mass is an environmentally driven effect, thus changes in body mass can be due to phenotypically plastic responses, in this case a population level response that affects all individuals. However, individuals differ in their genotypes, their ability to express a trait, and their ability to respond to environmental conditions. Furthermore, individuals can differ in their ability to compensate. Thus, within a population, individuals intrinsically vary in their June body mass, and some such individuals have relatively low weight compared to others in the same cohort. For these individuals, compensatory responses can be an important mechanism to catch up after a bad start following hibernation by growing faster than others. Thus, this compensatory response may have important, direct fitness consequences at the individual level, as well as indirect fitness consequences at the population level.
Section snippets
Study species
We studied yellow-bellied marmots in and around the Rocky Mountain Biological Laboratory (RMBL). Yellow-bellied marmots hibernate for 7–8 months annually (Armitage, 1991). Thus, they must gain sufficient body mass during their relatively short active season to survive hibernation. Reproduction, gestation and lactation take place during the active period (Armitage, 1991). Mating occurs in the spring, after emergence. Females do not start to reproduce until age two and, once they breed, they are
Baseline non-plasticity model
The Pearson's correlation test between the predicted and the observed λ shows that the parameters used in the baseline non-plasticity model provide a reasonably good match between predicted and observed lambda values (r = 0.573; 95% CI = 0.542–0.604) However, this result suggests that the baseline non-plasticity model has not captured all of the factors that affect the actual marmot population dynamics, and can be improved upon. Therefore, we would expect that if plasticity in growth rate were a
Discussion
We developed a stochastic, environmentally-driven, individually-based, demographic model for yellow-bellied marmots. This model allowed us to evaluate the effect of phenotypic plasticity in growth rates (i.e., compensatory growth) on population dynamics and persistence when we take into account variation in the plastic response among marmots, a cost for plasticity and the body mass conditions under which an individual can express plasticity at a given time. Our model showed that compensatory
Conclusion
In conclusion, by constructing individual-based models, we gained a deeper understanding of the role of individual differences in the mechanisms that govern population fluctuations in comparison to similarly structured population-level models, such as matrix projection models (MPM; Caswell, 2001) that assume uniformity across individuals. Our results highlight the role of compensatory responses as a mechanism by which individuals in poor body condition can cope with adverse environmental
Acknowledgements
We are very grateful to all the marmoteers who helped in the data collection, to K. Armitage for allowing us to use some of the historical data, and to the UCLA Statistical Consulting Group for their insights on the data analysis. A.M.-C. was supported by a Fulbright Fellowship, D.T.B was supported by the National Geographic Society, UCLA (Faculty Senate and the Division of Life Sciences), a Rocky Mountain Biological Laboratory research fellowship, and by the NSF (IDBR-0754247, DEB-1119660, and
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