Transgenerational Plasticity in Human-Altered Environments

Abstract

Our ability to predict how species will respond to human-induced rapid environmental change (HIREC) may depend upon our understanding of transgenerational plasticity (TGP), which occurs when environments experienced by previous generations influence phenotypes of subsequent generations. TGP evolved to help organisms cope with environmental stressors when parental environments are highly predictive of offspring environments. HIREC can alter conditions that favored TGP in historical environments by reducing parents' ability to detect environmental conditions, disrupting previous correlations between parental and offspring environments, and interfering with the transmission of parental cues to offspring. Because of the propensity to produce errors in these processes, TGP will likely generate negative fitness outcomes in response to HIREC, though beneficial fitness outcomes may occur in some cases.

Keywords: HIREC; climate change; human-induced rapid environmental change; maternal effects; parental effects; phenotypic plasticity.

Figure 1.. Overview of the Key Determinants of the Transgenerational Consequences of Human-Induced Rapid Environmental Change (HIREC) Using a Hypothetical Example.

Transgenerational plasticity (TGP) is a process by which offspring phenotypes are altered by environments experienced by previous generations (e.g., parents). Parental experiences can be conveyed to offspring through a variety of potential mechanisms, but TGP involves three general processes (top panel). In historical environments, TGP is more likely to be favored when these processes occur with minimal error. This is likely if: (i) parents possess the sensory/biochemical systems to accurately detect and identify environmental conditions and cue reliability is high, (ii) temporal/spatial environmental variability is low or similar to historic conditions and/or temporal/spatial autocorrelation is high, and (iii) parents can accurately transmit information about their environment to offspring and offspring can accurately integrate that information into their phenotype. Human-altered environments (bottom panel) increase the potential for errors in each of these processes. This may be due to the introduction of novel environmental conditions (which may reduce cue reliability), increases in environmental variability, or decreases in environmental autocorrelation relative to historic environments. HIREC may also increase the likelihood of mismatches between offspring phenotypes and human-altered environments and lead to detrimental effects of TGP. Visual example in both panels adapted from [66], who found that direct exposure to predator risk cues from dragonfly larvae cause tadpole prey to develop an antipredator phenotype (deeper tails) and that exposure to herbicides can elicit this same phenotypic response. We extend this WGP example to suggest possible errors in the process of TGP. Images by M. Bensky.

Figure I.. Potential Mechanisms of Transgenerational Plasticity.

Transgenerational plasticity can operate through a variety of mechanisms listed above that affect offspring at various stages of ontogeny, including at fertilization, during development/gestation, and after emergence. While some mechanisms are specifically linked to one stage of offspring development (e.g., epigenetic changes in gametes conveyed at fertilization), other mechanisms (e.g., parental state, niche construction) are relevant for offspring at multiple points in development. Regardless of when parental cues are delivered to offspring, many transgenerational plasticity mechanisms have lifelong effects on offspring.