The earth’s climate has changed multiple times at different time scales in the past, ranging from thousands to millions of years. Milankovitch’s cycles describe the collective effects of changes in the Earth’s movements upon its climate at predictable intervals of 10,000 to100,000 years [1], providing an important pacemaker for natural global climatic change over long time periods. Additionally, climate change occurs at different rates and periodicity (e.g., sporadically vs. cyclically) within this climatic oscillation, making climate change a constant feature of life on earth. When change is very slow (over many generations), individuals of a species can respond through evolutionary adaptation [2]. For example, animals can respond to changing conditions phenologically/physiologically (e.g., by changing the timing of life cycles [3]). Alternately, when change is very rapid and occurs during the lifetime of an individual, some individuals could respond through phenotypic plasticity [4]. For example, animal species can change morphologically (e.g., changes in tarsus length in collared flycatchers Ficedula albicollis [5]), behaviorally (e.g., migrating/shifting range [6]), or perhaps a combination of these (e.g., thermoregulatory behavior inhibits selection for changing thermal physiology in lizards Anolis cristatellus [7] but promotes morphological adaptation to facilitate locomotion, depending on the prevailing substrate [8]). In many species, organ size can change flexibly as a response to environmental changes, which can optimize energy acquisition [9]. Acclimatization to changing climatic conditions [10], as well as learning [11] are other important examples.

We are currently experiencing climate change that is unprecedented in the earth’s history, both in terms of the rapidity [12] and unpredictability of change (e.g., abrupt changes [13]), largely due to anthropogenic induced global warming. The rapid rate of current climate change is expected to severely impact ecosystems and their constituent organisms [14]. Coupled with other types of human-induced rapid environmental change, such as habitat loss/fragmentation, over-harvesting, pollution and the spread of invasive/exotic species, climate change will expose species to novel and unpredictable conditions [15], which will test the limits of their survival capability. This is why current climate change has been associated with increased probability of extinction [16]. For example, large scale global warming has shifted the growth optimum of Batrachochytrium dendrobatidis (a pathogenic chytrid fungus of amphibians), resulting in the disappearance (presumed extinction) of 73 species (67%) of harlequin frogs Atelopus sp. from Costa Rica in the last 25 years [17].

Those species that respond adaptively to change are of particular importance for scientific scrutiny to understand how species can cope with rapid, abrupt changes and thus avoid extinction. In this paper, we review how animal species displaying phenotypic flexibility have the potential to respond adaptively to and persist in rapidly changing environments. We review the mechanisms that underlie phenotypic flexibility, focusing particularly on behavioral flexibility. Our studies of the African striped mouse Rhabdomys spp. have been most revealing of how this taxon alters its behavior in response to prevailing environmental conditions, thereby making it a suitable model organism to understand flexibility as an adaptation to rapidly changing environments.

We first place our review in a broader context by defining terms and concepts that distinguish between alternative responses (Table 1) to predictable, long-term changes and rapid, short-term changes (Table 2). Specifically, we define the concepts of adaptation and phenotypic flexibility, in particular behavioral flexibility (Table 1). We then discuss how flexibility evolves and highlight the selection pressures that drive the expression of a flexible response when species encounter novel, unpredictable conditions. We show how behavioral flexibility promotes species persistence during periods of unpredictable, extreme environmental change, using the striped mouse as a model. Finally, we provide scenarios for the responses of striped mice to impending aridification in their geographic distribution in southern Africa.

It is important to distinguish behavioral flexibility (Table 1), which occurs when individuals change their behavior in response to changing environmental conditions [29], from other forms of behavioral variation [56]. Behavioral flexibility is characterized by observing variation in behavior within individuals, whereas other forms of behavioral variation consider differences between individuals (either genetic variation [57] or developmental plasticity). Activational hormonal effects and learning are two main mechanisms mediating behavioral flexibility. Activational effects are usually transient and reversible, serving to alter behavioral state in adulthood through modification of previously organized neural pathways [48], whereas learning is a process of modifying behavior through accumulated lifetime experience in response to environmental stimuli [58]. Species that are most likely to show behavioral flexibility, such as primates [59], tend to have bigger brains relative to body size [60] and/or have a greater tendency to display innovative behaviors [61]. These species also demonstrate a greater propensity to learn and acquire information from others [59].

Behavioral flexibility is advantageous under spatial and/or temporal heterogeneity ([58,62], Table 2) and evolves when the fitness benefits outweigh the costs [63]. For example, many species of tadpoles change their activity levels in response to increased perceived predation risk [64] and the number of predators in a system can fluctuate depending on a variety of other environmental factors (e.g., intraguild predation [65]). Therefore, in the face of environmental change, species that show flexible responses are likely to persist [66,67]. In fact, a greater disturbance is likely to promote the production of an even greater phenotypic response [68]. Species that are less flexible are more likely to emigrate [69] or, if they cannot respond, become extinct.

Social flexibility is a form of behavioral flexibility. It is characterized by the ability of individuals of both sexes within a population to switch between alternative reproductive and social tactics, depending on prevailing environmental and social conditions, causing the entire social system to change because of changing social interactions between individuals [70]. Thus, social flexibility is observed at the population level, due to individual flexibility in the social tactics of both sexes. This flexibility is possible because activational effects, and their associated neuroendocrine responses, drive the expression of alternative traits. Social flexibility is not based on genetic polymorphisms, but is rather a function of a fixed set of decision rules that all individuals follow under a given set of circumstances (genetic monomorphism [71]). In other words, both sexes of a population follow a single strategy and, depending on environmental conditions, switch between tactics, such as living alone or in groups. Environmental conditions determine the fitness consequences of adopting a particular tactic [70]. Because it occurs in a number of animals, including insects (e.g., burying beetles Nicrophorus vespilloides [72,73]), birds (e.g., dunnocks Prunella modularis [74]), and several species of rodents [70,75,76,77], social flexibility provides a unique opportunity for considering how species respond to environmental change.

Social flexibility allows for survival under changing environmental conditions. However, we need to consider how social flexibility operates at the individual and population levels to assess its contribution to survival. At the individual level, switching between social tactics is mediated by the endocrine system [53]. Hormones can alter physiological and behavioral responses [108], enabling individuals to switch between behavioral phenotypes. These patterns of hormonal secretion are sensitive to changes in environmental conditions. In R. pumilio, the three alternative male reproductive tactics are associated with changes in sex steroid hormones, in particular, testosterone, prolactin and corticosterone [105,109]. Philopatric males that leave their group increase their testosterone levels while at the same time decreasing their corticosterone levels, and philopatrics and roamers males that become paternal territorial breeders additionally increase their prolactin levels [110]. However, patterns of hormonal secretion can also be influenced during the early neonatal environment by the mother (i.e., maternal effects [108]), which influence behavior. In R. pumilio, solitary breeding females provide 1½ times more care to their young than paired females, resulting in their sons showing higher levels of paternal care as adults [111].

Although the decision rules for switching tactics are fixed in R. pumilio, decisions made at the individual level impact the population through social interactions, which cause changes in conspecific behavior [70]. Behavioral interactions, in turn, impact on how the population is organized (e.g., solitary vs. group-living), which then impacts individual decision making, resulting in a cyclical process that occurs regardless of the type and intensity of environmental disturbance. Group-living, and its associated energy savings due to huddling, increase R. pumilio survival during periods of food shortage (drought), whereas solitary living maximizes individual reproductive success after periods of increased mortality due to high food shortage, such that populations can recover quickly.

The evolved endocrine mechanisms that facilitate social flexibility will allow R. pumilio to respond to changing conditions faster than evolutionary adaptation ([18,70], Table 1). Moreover, since decisions made by individuals affect and are affected by the social organisation of the population, the spatial and temporal variability of population level effects (e.g., population size, reproductive tactics of some of the opposite sex) regulate decisions made by individuals, which are dynamic and reversible. The underlying strategies themselves are under selection pressure by the fitness consequences of the chosen tactics under the prevailing conditions. Therefore, social flexibility in R. pumilio might allow for its survival and persistence in unsustainable environments that experience unpredictable change [77].

Unlike R. pumilio, relatively little is known about the level of social flexibility of R. dilectus in its natural (moist grassland) habitats, but we have some evidence of behavioral flexibility from our captive studies. Although male R. dilectus show paternal care in the laboratory [94], the opportunity to show paternal care has not yet been demonstrated in nature, because males do not associate with females post mating. Thus, paternal behavior may be plesiomorphic in the genus and most likely arose in a desert-living ancestor similar to R. pumilio [81], where paternal care would be adaptive because of the advantages that the father provides for offspring development [99]. The occurrence of paternal care in captivity nonetheless suggests that male R. dilectus have the potential for displaying this behavior in nature, should conditions become appropriate for its expression (e.g., males remain with females post mating).

R. dilectus is more anxious than R. pumilio in open spaces, decreasing levels of exploratory behavior and increasing thigmotaxic responses [93], thereby displaying a comparatively shy personality. R. pumilio is bolder, preferring open spaces [93]. These differences between the species are also reflected in responses to novel food, with R. dilectus showing a slower response than R. pumilio [92]. The behavior of both species in open spaces and to novel environments is not fixed, however. We showed in a recent study that exploratory behavior in both species is modified by interspecific cross-fostering (i.e., offspring of one species raised by foster parents of the other species [93]). Interestingly, fostered striped mice of both species showed levels of exploratory behavior and anxiety intermediate to their biological and foster parents, demonstrating that exploratory behavior is flexible and influenced by an interplay of genetic predisposition and conditions during the early (ontogenetic) environment.

Our ongoing research into the social behavior of R. dilectus has revealed some unexpected findings. Same-sex dyadic encounters comprising unrelated females were largely amicable [112] and triads of related females form long-term stable groups [113], indicating a level of tolerance contrary to their solitary lifestyles in nature. Thus, R. dilectus females might have the potential to form communally breeding groups, regardless of whether or not they are related. Despite these tolerances, there is some indication of reproductive suppression among non-related females housed in close proximity (i.e., visual, auditory and olfactory contact, but no physical contact): dominant females increased their reproductive output and subordinates spent more time attending their pups [114].

The distribution of R. dilectus covers a vast geographic area in southern Africa, occurring in four different biomes (Figure 1), yet populations of the two subspecies R. d. dilectus and R. d. chakae show remarkably similar general activity patterns and exploratory behavior in captivity [112], and social organization in nature [86,100], despite occurring far apart geographically and in areas differing significantly in rainfall. Since the grasslands of South Africa are comparatively stable environments [83], it is possible that selection has favored relatively similar genotypes across a wide range of habitats.

The similarities in behavior in a number of populations of the R. dilectus subspecies indicate resilience to change, or stabilizing selection for behaviors that are optimal for striped mice in grasslands. If social flexibility indicates an ability to respond to unpredictable environmental change, the question that then emerges is: can R. dilectus display social flexibility? Behavioral flexibility and social tolerance are evident in this taxon but we do not know the extent and limits of this flexibility nor do we have a thorough understanding of the mechanisms underpinning flexibility in this species.

Southern Africa is predicted to become warmer (increase by at least 4 °C) and drier (decrease in annual precipitation by 10–20%) by the end of the century (Figure 2), resulting in increased risk of drought [115]. Based on our long-term research of Rhabdomys spp reviewed above, we provide three scenarios about the persistence of its constituent taxa under predicted environmental change. As the majority of climate change models (e.g., HadAM3H, [116]; IPCC A1B, [115]; RCM, [117]) predict conditions far into the future, we chose to follow a similar convention by using the Africa-specific model from Collier et al. [115]. Our three scenarios relating to either extinction, range shift or persistence are in accordance with the predicted pace of climate change (modeled at [118] using the SRES_A1B emission scenario). These scenarios have heuristic value when viewed separately, but they are not mutually exclusive because there is a strong likelihood that all may occur simultaneously.

Our study organism, Rhabdomys pumilio, displays an ability to switch social tactics (i.e., social flexibility), which is a form of behavioral flexibility. Behavioral flexibility is an adaptive response that can promote species persistence in the face of unpredictable, unstable and novel environmental change. Such flexibility possibly contributes to the persistence of R. pumilio currently in arid habitats and could result in range expansion because of predicted habitat change (aridification) and severe human-induced rapid environmental change in southern Africa. Whether other species of Rhabdomys are able to mount a similar response is unknown and will determine their survival or extinction in their current habitats. The extent to which plasticity and flexibility in other traits are important for survival is another important topic to study. We expect that physiologically flexibility, such as acclimatization and reduction of resting metabolic rate, can be important to survive drought periods. Further, organ sizes (e.g., respirometry, digestive) might change significantly, as observed in other species [9], and facilitate adaptation to a changing environment. Thus, while social flexibility is very important for striped mice to respond to change, other mechanisms might be additionally at play.

Behavioral flexibility is costly since it relies on the development and maintenance of neural structures that are involved in learning and memory [124] or maintenance of sensory and response pathways involved in inducing a plastic response [58]. The ability to display flexibility is thus expected to show evolutionary trade-offs with other fitness-related traits, and the costs of behavioral flexibility might be incurred regardless of whether or not flexibility is expressed [58]. However, since phenotypes are likely to change in response to environmental disturbance without a corresponding change in the genotype [9], survival and persistence is possible in the short-term, which would overcome the costs associated with demonstrating phenotypic flexibility. In the long-term, specific phenotypic traits could become fixed through evolutionary adaptation, although the role of phenotypic plasticity in evolutionary diversity is generally debated [4].

Several studies address the possibility of species adaptation to global change via evolutionary adaptation (evolutionary rescue [125]) and others model the extinction risk for populations [126,127]. However, how individuals will persist in the face of change is currently unknown. Ultimately, the survival, reproduction and extinction of populations and species are dependent on the probability of survival of individuals, a topic that has received little, if any, attention. Since the survival of individuals is determined by their ability to adapt and respond to change, there needs to be an understanding of the limits to phenotypic adaptation, such as starvation and reduced physical and cognitive ability, if we are to understand whether populations as a whole can respond to environmental change.

Using the different species of Rhabdomys as models, we outlined here that animal species with phenotypic flexibility, in particular social (behavioral) flexibility, are more likely to survive rapid environmental changes. Although the scenarios presented are specific to our model, we suggest that these could apply to other taxa with distributions encompassing many different environments/biomes. Future studies should investigate whether social flexibility is a toolkit for survival in other species, as well as how the absence of social flexibility could be a constraint for survival under anthropogenic climate change.