Evidence base for non-genetic inheritance of environmental exposures in non-human animals and plants: a map of evidence syntheses with bibliometric analysis

Abstract

Background Direct effects of parental environment (particularly mothers) on offspring have been frequently demonstrated over the last decades. More recently ‘indirect’ non-genetic effects of ancestral environment and environmental effects through the patriline have been observed. Such research has captured the interest of many disciplines including biomedical science, toxicology, agriculture, and ecology and evolution due to the importance of understanding environmental effects on individual and population health. Consequently, the secondary literature, aimed at synthesizing non-genetic effects has also been increasing. The non-genetic inheritance secondary literature can be as diverse as the primary literature. Thus, there is a need to ‘map’ the non-genetic inheritance secondary literature to understand the state of the field and move forward in filling research gaps. Here, we ask four main questions: (1) What evidence exists on the impacts of non-genetic inheritance in non-human animals and plants across disciplines within the secondary ‘systematic-like’ (evidence synthesis) literature (2) What are the discipline-specific research patterns and gaps? (3) How connected is the literature (i.e., shared citations within and between disciplines, and collaborations between different countries)? (4) What is the overall quality of the non-genetic inheritance SR literature? Methods We systematically searched for published and grey evidence syntheses on non-genetic inheritance in non-human animals and plants. We then extracted details pertaining to research topics and assigned each article to one of five disciplines (agriculture, biomedical science, ecology and evolution, toxicology, and cross-disciplinary research). We mapped within- and between- discipline research patterns through descriptive statistics and visualizations, and conducted a bibliometric analysis of the ‘connectedness’ of the literature (i.e., co-citation and collaboration networks). We also conducted a critical appraisal of the included articles. Results We show that most evidence syntheses were in biomedical science and synthesized primary literature on rats and mice. Most evidence syntheses examined ‘direct’ effects of ancestral environment on descendants, particularly maternal dietary effects on offspring physiology and morphology. Ecology and evolution and cross-disciplinary evidence syntheses included the most diverse range of primary literature in their articles. We also show that most evidence syntheses have at least one author affiliated with an institution in the USA, and that the UK tends to form the most multinational collaborations. Toxicology evidence syntheses were least likely to cite studies outside of its own discipline. Lastly, we show where the quality of the non-genetic inheritance systematic-like literature could be improved. Conclusions We have highlighted that certain areas of non-genetic inheritance are more frequently synthesised than others which may reflect a stronger interest in certain research topics at either the secondary or primary literature level. Presenting these research patterns and gaps in the literature that will not only make it easier to for researchers to understand the current state of the literature, but will also aid in bridging gaps between disciplines in the future. This will have substantial benefits for our understanding of non-genetic inheritance, with implications for many research fields, including climate change research, ecological and evolutionary theory, and understanding the effects of environmental pollutants on population health. It will also help policy makers identify relevant literature to inform policies, especially related to the negative impacts of environmental factors across generations.

Sixty years since Silent Spring: a map of meta-analyses on organochlorine pesticides reveals urgent needs for improving methodological quality.

“…However, we found that across all methodological areas assessed by CEESAT v2.1, Green (10.7%) and Gold (5.9%) scores remained scarce. This finding is consistent with other reports that poor-quality methodologies are common in environmental science (L. Macartney et al, 2023;Menon et al, 2022;Nakagawa et al, 2023b). For complete details on the results of each CEESAT v2.1 item, please see Supplementary File 1, Objective 1.…”