The Logic of Transgenerational Inheritance: Timescales of Adaptation

Abstract

Myriad mechanisms have evolved to adapt to changing environments. Environmental stimuli alter organisms’ physiology to create memories of previous environments. Whether these environmental memories can cross the generational barrier has interested scientists for centuries. The logic of passing on information from generation to generation is not well understood. When is it useful to remember ancestral conditions, and when might it be deleterious to continue to respond to a context that may no longer exist? The key might be found in understanding the environmental conditions that trigger long-lasting adaptive responses. We discuss the logic that biological systems may use to remember environmental conditions. Responses spanning different generational timescales employ different molecular machineries and may result from differences in the duration or intensity of the exposure. Understanding the molecular components of multigenerational inheritance and the logic underlying beneficial and maladaptive adaptations is fundamental to understanding how organisms acquire and transmit environmental memories across generations. Expected final online publication date for the Annual Review of Cell and Developmental Biology, Volume 39 is October 2023. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.

Transgenerational epigenetic inheritance increases trait variation but is not adaptive

“…Non-genetic mechanisms of inheritance, broadly classified as ‘intergenerational’ or ‘transgenerational’, represent distinct biological pathways 11 and could play an important role in the transmission of heritable phenotypic changes in response to environmental fluctuations 12 . Intergenerational inheritance involves the transfer of traits from parent to offspring through mechanisms independent of inherited DNA modifications, such as the acquisition of epigenetic marks during in utero development in live birth species and non-epigenetic mechanisms like maternal resource provisioning 11,13,14 . Conversely, transgenerational inheritance involves the transmission of epigenetic information across multiple generations that can persist even in the absence of the original environmental stimulus—known as transgenerational epigenetic inheritance (TEI).…”

“…This assumption stems from the central dogma of genetics: differential DNA methylation patterns or histone modifications influence gene regulation in a direction that enhances fitness that could conceivably improve population persistence in changing environments 10,31–35 . Testing the veracity of these adaptive assumptions requires measurements made in the F3 generation or beyond 11,15,16,26 to disentangle inherited epigenetic modifications from parental and non-inherited changes. To date, the limited number of studies measuring the phenotypic effects of TEI in the F3 and later generations 27,36 makes drawing definitive conclusions about its effects on phenotypes and fitness tenuous.…”

“…Conversely, transgenerational inheritance involves the transmission of epigenetic information across multiple generations that can persist even in the absence of the original environmental stimulus—known as transgenerational epigenetic inheritance (TEI). The most studied underlying mechanisms of TEI are differential patterns of DNA methylation, histone modifications, and the transmission of non-coding RNAs 11,15,16 . Despite methodological advances leading to a better understanding of inherited epigenetic marks associated with a variety of stressors across taxa 17–19 , the true impact of epigenetic modifications on organismal phenotypes and population-level responses remains largely unknown.…”

A natural bacterial pathogen of C. elegans uses a small RNA to induce transgenerational inheritance of learned avoidance

“…These changes can occasionally cross the germline and confer adaptive benefits to the first generation of progeny (intergenerational) [7][8][9][10][11][12][13][14][15][16][17][18][19][20] or more (transgenerational) [21][22][23][24][25][26][27][28][29][30][31][32][33]. Multigenerationally-inherited effects can provide adaptive advantages in changing environments, particularly in organisms with short generation times [34][35][36].…”

A natural bacterial pathogen ofC. elegansuses a small RNA to induce transgenerational inheritance of learned avoidance

“…These changes can occasionally cross the germline and confer adaptive benefits to one generation of progeny (intergenerational) (Burton et al, 2021(Burton et al, , 2020(Burton et al, , 2017Conine et al, 2018Conine et al, , 2013Guida et al, 2019;Hibshman et al, 2016;Hong et al, 2021;Jordan et al, 2019;Lim et al, 2021;Ow et al, 2021;Pereira et al, 2020;Perez et al, 2021;Willis et al, 2021) or more (transgenerational) (Gammon et al, 2017;Jobson et al, 2015;Kaletsky et al, 2020;Legüe et al, 2022;Mondotte et al, 2020;Moore et al, 2021Moore et al, , 2019Rechavi et al, 2014Rechavi et al, , 2011Toker et al, 2022;Vogt and Hobert, 2023;Wang et al, 2022;Webster et al, 2018). Multigenerationally-inherited effects can provide adaptive advantages in rapidly changing environments, particularly in organisms with short generation times (Baugh and Day, 2020;Sengupta et al, 2023;Uller et al, 2015).…”