The ecology of environmental DNA and implications for conservation genetics

Abstract

Environmental DNA (eDNA) refers to the genetic material that can be extracted from bulk environmental samples such as soil, water, and even air. The rapidly expanding study of eDNA has generated unprecedented ability to detect species and conduct genetic analyses for conservation, management, and research, particularly in scenarios where collection of whole organisms is impractical or impossible. While the number of studies demonstrating successful eDNA detection has increased rapidly in recent years, less research has explored the ''ecology'' of eDNA-myriad interactions between extraorganismal genetic material and its environment-and its influence on eDNA detection, quantification, analysis, and application to conservation and research. Here, we outline a framework for understanding the ecology of eDNA, including the origin, state, transport, and fate of extraorganismal genetic material. Using this framework, we review and synthesize the findings of eDNA studies from diverse environments, taxa, and fields of study to highlight important concepts and knowledge gaps in eDNA study and application. Additionally, we identify frontiers of conservation-focused eDNA application where we see the most potential for growth, including the use of eDNA for estimating population size, population genetic and genomic analyses via eDNA, inclusion of other indicator biomolecules such as environmental RNA or proteins, automated sample collection and analysis, and consideration of an expanded array of creative environmental samples. We discuss how a more complete understanding of the ecology of eDNA is integral to advancing these frontiers and maximizing the potential of future eDNA applications in conservation and research.

Attracting Common Carp to a bait site with food reveals strong positive relationships between fish density, feeding activity, environmental DNA, and sex pheromone release that could be used in invasive fish management

“…Most importantly, it suggests that there may not always be a simple linear relationship between wild fish biomass and eDNA concentration because behavior is factor (Barnes & Turner, 2016). Other behaviors may have similar effects on eDNA, especially spawning (Erickson et al., 2016).…”

“…Other behaviors may have similar effects on eDNA, especially spawning (Erickson et al., 2016). Finally, while our finding that eDNA rapidly dissipated within just 5 m reinforces our previous results (Eichmiller et al., 2014) as well as numerous laboratory studies (Barnes & Turner, 2016; Eichmiller et al., 2016; Lance et al., 2017; Turner et al., 2014) which describe rapid decay and binding; further research is needed to precisely estimate degradation rates and the many factors that likely influence it in natural waters, especially in rivers.…”

“…Nevertheless, surveying for fish using the DNA they release (environmental DNA or “eDNA”) has become a method of choice because of the sensitivity and specificity of the technique, and the ease with which water can be collected (Bylemans et al., 2017; Ficetola, Miaud, Pompanon, & Taberlet, 2008; Jerde et al., 2011; Lacoursière‐Roussel, Rosabal, & Bernatchez, 2016; Minamoto et al., 2017; Taberlet, Coissac, Hajibabaei, & Rieseberg, 2012; Takahara, Minamoto, Yamanaka, Doi, & Kawabata, 2012; Thomsen & Willerslev, 2015). However, the utility of measuring eDNA is presently limited by the fact that many basic tenants of the ecology of eDNA are not well understood (Barnes & Turner, 2016; Evans & Lamberti, 2018). In particular, little is understood about either the origins of eDNA or factors that drive its release.…”

“…In particular, little is understood about either the origins of eDNA or factors that drive its release. Additionally, while our understanding of eDNA degradation, dilution and binding has expanded in recent years (Barnes & Turner, 2016; Evans & Lamberti, 2018; Turner et al., 2014), exactly how these factors interact to determine the distribution and fate of eDNA released by free‐ranging fish in natural waters remains unresolved. Finally, eDNA does not provide any information on whether fish are alive.…”

“…While eDNA measurement is proving to have value to managers, it nevertheless is limited because it does not, and cannot, provide information on fish gender, reproductive condition, or health; indeed, dead fish also shed eDNA (Barnes & Turner, 2016). However, pheromones, chemicals which fish release to convey taxon‐specific information (Sorensen & Wisenden, 2015) naturally provide this information about fish.…”