Can environmental conditions experienced in early life influence future generations?

Abstract

The consequences of early developmental conditions for performance in later life are now subjected to convergent interest from many different biological sub-disciplines. However, striking data, largely from the biomedical literature, show that environmental effects experienced even before conception can be transmissible to subsequent generations. Here, we review the growing evidence from natural systems for these cross-generational effects of early life conditions, showing that they can be generated by diverse environmental stressors, affect offspring in many ways and can be transmitted directly or indirectly by both parental lines for several generations. In doing so, we emphasize why early life might be so sensitive to the transmission of environmentally induced effects across generations. We also summarize recent theoretical advancements within the field of developmental plasticity, and discuss how parents might assemble different ‘internal’ and ‘external’ cues, even from the earliest stages of life, to instruct their investment decisions in offspring. In doing so, we provide a preliminary framework within the context of adaptive plasticity for understanding inter-generational phenomena that arise from early life conditions.

An ontogenetic perspective on individual differences

“…The existence of a 'window' after which a trait is no longer plastic reinforces our general understanding of development from conception to adulthood as a linear process punctuated by changes in an individual's experienced environment (e.g. birth) that act as borders between ontogenetic stages [7,8]. Determining precisely when an individual difference arises is fundamental to identifying its source, as well as predicting its consequences (figure 1).…”

“…Because most life-history stages progress linearly, each life-history event in these stages only occurs once (adulthood in iteroparous organisms is the exception and will be discussed later). This dictates that each individual difference that arises will probably affect the outcome of the next developmental step, codifying and potentially exacerbating its downstream phenotypic effects (figure 1) [2,7,8,38]. Most, but not all [39], individual differences originating during development are therefore permanent and can result in altered reproductive success throughout an individual's life [8].…”

“…This variation arises from various sources-genetic, parental and environmental-and may result in long-term or ephemeral inter-individual differences [1][2][3][4][5][6]. The life-history stage during which such differences originate influences both the period of time over which they are maintained and their likelihood of affecting individual fitness [7][8][9]. As a result, individual differences arising in different ontogenetic stages have unique qualities; we thus refer to each as a 'type' of individual difference (see table 1).…”

Rapid adaptive responses to climate change in corals

“…For example, adaptive TGP might be expected when the parental environment is a reliable predictor of environmental conditions that their offspring will experience 53,54 . Because short-range offspring dispersal typically enhances environmental predictability among generations 55 , the benefits of TGP are expected to be inversely proportional to the dispersal capacity of the organism.…”

Observational field studies reveal wild birds responding to early-life stresses with resilience, plasticity, and intergenerational effects

“…Although seldom sought, these have been documented in diverse taxa (Burton and Metcalfe 2014), including 4 species of birds. Application of experimental stresses to captive nestlings or juveniles induced deficits in their offspring: diminished size, hatching success, and nest success in female Zebra Finches (Naguib and Gil 2005, Naguib et al 2006, Alonso-Alvarez et al 2007); reduced spatial learning or corticosterone responsiveness in breeds of Domestic Fowl (Lindqvist et al 2007, Goerlich et al 2012; and increased fearfulness in Japanese Quail (Guibert et al 2012).…”