Parallel and nonparallel genomic responses contribute to herbicide resistance in Ipomoea purpurea, a common agricultural weed

Abstract

The repeated evolution of herbicide resistance has been cited as an example of genetic parallelism, wherein separate species or genetic lineages utilize the same genetic solution in response to selection. However, most studies that investigate the genetic basis of herbicide resistance examine the potential for changes in the protein targeted by the herbicide rather than considering genome-wide changes. We used a population genomics screen and targeted exome re-sequencing to uncover the potential genetic basis of glyphosate resistance in the common morning glory, Ipomoea purpurea, and to determine if genetic parallelism underlies the repeated evolution of resistance across replicate resistant populations. We found no evidence for changes in 5-enolpyruvylshikimate-3-phosphate synthase (EPSPS), glyphosate's target protein, that were associated with resistance, and instead identified five genomic regions that showed evidence of selection. Within these regions, genes involved in herbicide detoxification-cytochrome P450s, ABC transporters, and glycosyltransferasesare enriched and exhibit signs of selective sweeps. One region under selection shows parallel changes across all assayed resistant populations whereas other regions exhibit signs of divergence. Thus, while it appears that the physiological mechanism of resistance in this species is likely the same among resistant populations, we find patterns of both similar and divergent selection across separate resistant populations at particular loci.

The role of population and quantitative genetics and modern sequencing technologies to understand evolved herbicide resistance and weed fitness

“…[10][11][12] The literature has abundant cases of target site resistance, while fewer studies on NTSR have been published. 3,9,13 This is due to the fact that single genes (i.e. monogenic) commonly associated with target site resistance often cause large phenotypic differences between resistant and susceptible individuals that are easily identified in the field, especially when exposed to high herbicide rates.…”

Rapid Parallel Adaptation to Anthropogenic Heavy Metal Pollution

“…Rapid habitat loss or environmental change can drive species to the brink of extinction, but also presents opportunities for adaptation and speciation (Johnson & Munshi-South 2017;Otto 2018;Ravinet et al 2018;Szulkin, M., Munshi-South, J., & Charmantier 2020). There are numerous examples of rapid adaption to human-modified landscapes or activities (McNeilly & Bradshaw 1968;Antonovics & Bradshaw 1970;Wu & Bradshaw 1972;Macnair 1979;Hof et al 2016;Reid et al 2016;Bosse et al 2017), but there is a relatively limited understanding of the extent to which this process is repeatable and predictable (Bay et al 2018;Fitzpatrick et al 2018;Therkildsen et al 2019;Santangelo et al 2020;Van Etten et al 2020). It is also unclear whether such rapid evolution in the wild is typically facilitated by new mutations or draws on standing genetic variation, although there is increasing evidence for the role of standing variation in adaptation generally (Barrett & Schluter 2008;Thompson et al 2019).…”

“…Typically taking place tens of thousands or more years ago, such parallel evolution of ecotypes is well known in animals (Soria-Carrasco et al 2014;Ravinet et al 2016;Schweizer et al 2019;Jacobs et al 2020) with fewer clear examples in plants (Roda et al 2013;Trucchi et al 2017;James et al 2020). As a result, there are very few instances in which this kind of parallel adaptation is thought to have taken place rapidly in response to anthropogenic environmental change (Reid et al 2016;Alves et al 2019;Van Etten et al 2020). A significant complication in discriminating between a single or parallel origin of an ecotype (i.e., populations adapted to a specific habitat) is that local gene flow between divergent ecotypes can obscure the true evolutionary relationships of the populations (Ravinet et al 2016;James et al 2020).…”

“…Instances where the same toxic chemicals and contaminants have been repeatedly introduced into the environment by humans in isolated locations can generate novel selection regimes that have the potential to promote parallel adaptation. Strong selection, caused by herbicides, pesticides and heavy metals that contaminate soils and water bodies, is capable of producing extremely rapid adaptive responses (Antonovics & Bradshaw 1970;Wu & Bradshaw 1972;Macnair 1979;Hartley et al 2006;Van Etten et al 2020) and trade-offs (Xie & Klerks 2004), and may be particularly prone to triggering parallel responses as a result (MacPherson & Nuismer 2017). Indeed, there is evidence for rapid parallel adaptation from 'ancient' standing genetic variation during adaptation to copper mine contamination in two populations of Mimulus guttatus (Wright et al 2015;Lee & Coop 2017).…”

“…The mutations underlying this resistance have evolved on at least two occasions, but migration between three of the four populations may have contributed to the spread of tolerance (Lee & Coop 2017). Convergent herbicide resistance across species is well documented, but there is more limited support for parallel origins within single species and the spread of resistance by gene flow has been harder to rule out (Van Etten et al 2020).…”