Nongenetic inheritance is a potentially important but poorly understood factor in population responses to rapid environmental change. Accumulating evidence indicates that nongenetic inheritance influences a diverse array of traits in all organisms and can allow for the transmission of environmentally induced phenotypic changes (‘acquired traits’), as well as spontaneously arising and highly mutable variants. We review models of adaptation to changing environments under the assumption of a broadened model of inheritance that incorporates nongenetic mechanisms of transmission, and survey relevant empirical examples. Theory suggests that nongenetic inheritance can increase the rate of both phenotypic and genetic change and, in some cases, alter the direction of change. Empirical evidence shows that a diversity of phenotypes – spanning a continuum from adaptive to pathological – can be transmitted nongenetically. The presence of nongenetic inheritance therefore complicates our understanding of evolutionary responses to environmental change. We outline a research program encompassing experimental studies that test for transgenerational effects of a range of environmental factors, followed by theoretical and empirical studies on the population‐level consequences of such effects.

Bet‐hedging There is some evidence to suggest that mothers may adaptively adjust within‐brood variability of offspring phenotype in unpredictable environments, thereby increasing the likelihood that at least some of their offspring will have the ‘right’ phenotype in a changing environment (Crean and Marshall 2009). Mothers may also hedge their bets in unpredictable environments by producing offspring of higher quality than would be selected for in stable environments, thereby maximizing the chance of survival in any environment (conservative bet‐hedging: Einum and Fleming 2004). Evidence for plasticity in within‐brood variance as an adaptive strategy in unpredictable environments is mainly theoretical (e.g. Marshall et al. 2008; Olofsson et al. 2009), as the indirect and multi‐generational benefits of bet‐hedging are difficult to quantify empirically. However, the diversity of traits and range of taxa with anecdotal evidence of bet‐hedging suggests that it is widespread (Simons 2011), and thus adaptive plasticity in within‐brood variability may increase the likelihood that populations will persist under climate change.

Behavioral responses to altered environments Vertical transmission of behavioral variation (a form of ‘social inheritance’) may help populations adapt to environmental change if a novel behavior facilitates the use of a novel environment or provides a new way of interacting with the environment (Wcislo 1989; Duckworth 2009). Transmission of learned behavior to offspring enables immediate and adaptive responses to environmental variation, and consequently learned behaviors can allow populations to adapt quickly during periods of rapid environmental change. Some of the strongest evidence for vertical transmission of behavior is cone stripping by Israeli black rats, where cross‐fostering experiments showed the ability to strip pine cones efficiently is learned from mothers and not genetically determined (Aisner and Terkel 1992). Another example of behavioral inheritance facilitating the use of novel environmental niches is the matrilineal transmission of tool use in bottlenose dolphins. A subset of the population of bottlenose dolphins in Western Australia carry marine sponges over their rostra like a protective glove while probing the sea floor for prey (Krutzen et al. 2005). This foraging technique is behaviorally transmitted, mainly from mother to daughter (Krutzen et al. 2005; Bacher et al. 2010), and appears to allow females to exploit a lower quality foraging habitat with no apparent fitness costs (Mann et al. 2008). Therefore, nongenetic inheritance of foraging techniques may help populations cope with environmental change by decreasing feeding competition and facilitating the exploitation of novel food sources. However, behavioral plasticity (and therefore presumably behavioral inheritance) may also slow rather than promote evolutionary change by reducing the genetic covariance between behavioral phenotype and fitness (Huey et al. 2003; Duckworth 2009).

Pollution resistance Mothers exposed to anthropogenic pollution may transfer resistance to offspring. For example, in the marine bryozoan Bugula neritina, mothers exposed to copper (a common marine pollutant from antifouling paints) produce offspring that are more resistant to copper than larvae from copper‐naive mothers (Marshall 2008). Interestingly, larvae with an induced copper‐resistant phenotype were also more resistant to predation by flatworms (Moran et al. 2010), suggesting that nongenetically inherited resistance to pollution may have multiple indirect fitness benefits to offspring. However, offspring from copper‐exposed mothers suffered a fitness cost in the absence of copper, showing lower post‐metamorphic growth and survival compared with copper‐susceptible phenotypes (Marshall 2008). This effect was exacerbated when larvae were exposed to additional environmental stress, with a greater proportion of offspring from copper‐naive mothers surviving low salinity conditions compared with copper‐resistant offspring (Moran et al. 2010). Similarly, larval fish from mothers exposed to contaminated sediment were larger and had higher survivorship when also exposed to contaminated sediment, but suffered a fitness cost when reared on reference sediment (Nye et al. 2007). Hence, if current pollution exposure is an accurate predictor of future exposure to pollution, nongenetic transmission of pollution resistance to offspring is likely to help populations persist in an increasingly polluted environment. Conversely, if maternal pollution exposure is a poor predictor of offspring pollution exposure, induced resistance may actually have a detrimental effect on population persistence. The proximate mechanisms mediating these examples of transgenerational plasticity remain to be determined.

Conclusions Theoretical and empirical studies suggest that nongenetic inheritance is a potentially important factor in the fate of populations faced with rapid environmental change. Several complications remain to be resolved, however. First, short‐term effects of nongenetic inheritance on offspring fitness may not reflect longer‐term effects on population persistence and adaptation. Second, empirical evidence points to the nongenetic inheritance of a wide variety of induced pathological states. Such effects, which have not yet been examined in theoretical studies, could accelerate the demise of populations confronted by toxic pollutants or other environmental insults, but also perhaps increase the efficiency of selection against the most susceptible genotypes. Experiments to uncover the range of environmental factors with transgenerational effects, combined with modeling and multi‐generational studies on laboratory and natural populations, will illuminate the consequences of nongenetic inheritance for adaptation.

Acknowledgements We thank the special issue editors for inviting us to contribute this paper. RB and AJC were funded by an Australian Research Council Discovery Grant and Research Fellowship (RB), and TD was funded by the Natural Sciences and Engineering Research Council of Canada (NSERC), an NSERC Steacie Fellowship, and the Canada Research Chairs Program.