Knowledge about crop ancestors can illuminate the evolutionary origins of these problematic plants. Because of their economic importance, domesticated plants are often extraordinarily well-studied and well characterized; many are among the best studied plants. Consider this dramatic illustration: Of the hundreds of thousands of described plant species, roughly 1% are domesticated, but of the eight completely sequenced plant genomes, five belong to domesticated plants . Likewise, domesticated species are attractive for many evolutionary biologists. Charles Darwin’s The Variation of Animals and Plants under Domestication was published less than a decade after his On the Origin of Species by Means of Natural Selection . Most domesticated species are easily available for experimental and descriptive genetic comparison with their wild descendants. Thus, the history of crop descendants can often be reconstructed in some detail. For recently appearing weedy or invasive lineages, historic ethnobotanical information, confirmed by genetic data, can assign their geographic origin to a limited region. Similar information can sometimes be employed to determine which crop subspecies or varieties might have been involved in the origin of the troublesome lineage. Furthermore, drying marijuana domesticated plants are selected to be grown easily. For example, annual crop seeds typically exhibit no dormancy .
This tractability can facilitate common garden experiments to identify significant evolutionary changes that correlate with weediness or invasiveness. Despite these apparent advantages as well as a recent major treatment on crop ferality , plants with domesticated ancestors remain a largely underappreciated resource for studying how problem plants evolve. Our original motivation was to understand how natural selection works on the descendants of domesticated species so that they are able to become weedy or invasive. We were hoping to review the literature and accumulate a large number of examples to determine sweeping evolutionary generalizations such as whether natural selection results in, for example, the evolution of locally adaptation, of increased competitive ability, or of better dispersal. Below we identify the best studied systems, those invasive and weedy plants that have been genetically confirmed as descendants of domesticates. We found enough examples to identify some potential trends, but too few to make the broad generalizations that we had hoped for. Following our general review, we chose a few examples that provide some insights into the work that needs to be done on systems such as these. In particular, in our discussion, we look to the future. We identify plant pests that are worthy of more evolutionary scrutiny. We also consider how information from already characterized crop traits might illuminate which and how genes evolve along the route to pest status.
Finally, we discuss a number of research questions in evolutionary biology that might be fruitfully pursued in these study systems.We sought cases that demonstrate the evolution of invasiveness and/or weediness in plants with domesticated ancestors. We used four criteria for choosing our examples: 1 We considered only cases involving ancestors that are well-domesticated taxa. Here, we define well-domesticated taxa as those that have been intentionally cultivated for at least 1000 years. This initial filter limits the potential number of cases to several hundred species while eliminating most ornamentals, timber trees, and forage grasses. Compared to highly-domesticated plants that are well-differentiated from their wild ancestors, weakly-domesticated taxa are genetically so close to their wild ancestors that it would be almost impossible to determine whether their problematic descendants from have undergone any significant evolutionary change. To illustrate, Lantana camara is a plant famous in the nursery trade for escaping cultivation to become a globally significant invasive . But it is not clear that the either the horticultural varieties of L. camara or their invasive descendants are substantially genetically different from the original wild L. camara populations that are the original ancestors to both. We started out search by examining the examples in Gressel’s edited tour de force on crop ferality. Likewise, Andersson and de Vicente’s book on crops and their wild relatives provides detailed information on what is known about feral, weedy, and invasive lineages that have emerged from the world’s most important crop species.
Some other examples came from prior treatments that focused on exoferality .We found 13 examples of plant pest lineages are descended from crop progenitors. These are enumerated in Table 1. Ten are primarily noxious weeds of agriculture, one is an invader of non-managed ecosystems, and the remaining two are both weedy and invasive. Six have an endoferal ancestry; six are descended from hybrids between a domesticated taxon and a wild relative. In the remaining case, the plant pest lineage is descended from hybrids between two cultivated taxa. Two of the studies contributing to our list found both a crop origin and a noncrop origin for what has been considered to be a single taxon; that is, some, but not all, of the populations studied had crop ancestors. With regards to weedy rice in the United States, Londo and Schaal found that most of the accessions genetically analyzed and compared with an array of putative ancestors were either descended from hybrids or from the crop . But a single accession from California appeared to be descended directly from the wild ancestor O. rufipogon. In the similar study of wild artichoke thistle in California , of the 12 wild populations analyzed, four were found to have domesticated ancestry and eight were found to be descendants of Old World wild artichoke thistle. The list in Table 1 is diverse. The plants are annuals and perennials whose seed and pollen are dispersed in a variety of ways. Cultivated progenitors include both agronomic and horticultural crops. Given the importance of the grass family for human sustenance, it is not surprising that most of the examples are from that family. A few generalizations are apparent. With the exceptions of rice and wheat with endoferal ancestry, all other cases involve at least one parent that is predominantly outcrossing; in most of the cases at least one parent is self-incompatible. It is certainly possible that outcrossing could facilitate the recombination of genetic diversity between previously isolated lines, creating a burst of variation that can generate an array of phenotypes for a selective substrate . Whether this generalization will hold up as more systems are studied remains to be seen. Also, many of the reported evolutionary changes represent de-domestication, the evolutionary loss of traits accumulated under domestication . Nine of our examples show an evolutionary shift to readily dispersed seeds or fruits. Typically, agronomic crops that are grown for their seeds have evolved under human selection to be ‘non-shattering;’ that is, the infructescence or fruit holds seeds on the plant until harvest . The wild ancestors of those crops have the ‘shattering’ trait for dispersal. So, too, do more than half of our examples,indicating the evolutionary reversal of this trait in the successful derived populations. Three of our examples display the evolution of increased seed dormancy relative to their crop ancestors. Some dormancy in the wild is the rule for monocarpic plants; it has long been interpreted as an evolutionary ‘bet-hedging’ strategy by plant evolutionary ecologists . As noted above, domesticated annual crops typically have no dormancy, an anthropogenic adaptation that permits quick and uniform germination when sown . In at least one case, the key evolutionary change from a domesticated plant to a pest did not involve the evolutionary reversal of de-domestication.
Cultivated radish in southern Brazil has evolved resistance to ALS-inhibiting herbicides, the herbicides of choice in that region for no-till agriculture . The resulting lineage called ‘forrageiro’, is now a weed of both winter and summer crops. That trait is not present either in the crop or in its progenitors; thus, its evolution is not a case of de-domestication. In contrast with the examples of divergence from domesticated ancestors discussed above, cannabis drying rack in some of our cases certain domesticated traits are retained in the feral lineages. Those traits have not evolved because they presumably provide an evolutionary advantage. In particular, several of the cases in Table 1 are successful because they retained traits making them functional crop mimics. Weedy rice, weedy beet, weedy rye, and semi-wild wheat are hard to control because until they flower, they are morphologically hard to distinguish from their relatives. Thus, their survival is enhanced under hand-weeding. One of the two most significant generalizations is that the list is short. As we worked our way through the 25 contributed chapters of Crop Ferality and Volunteerism , we were surprised that many of the treatments of feral plants offered only agronomic and ecological detail, but very little insight into whether they had evolved from their cultivated ancestors. We contend that the other significant generalization is that there is much to learn from these systems. With few exceptions, our list is simply a recounting of studies that combine data from genetic markers with ethnobotanical history to establish that problem plants evolved from domesticates. Even data regarding the traits that make these plants problematic are largely superficial. However, we found three systems worthy of deeper discussion. First, we highlight the evolution of weedy rice because it illustrates how what is often perceived as a single problematic lineage is, in fact, a polyphyletic set of lineages with a diversity of evolutionary pathways that capture the breadth of how plant pests evolve from crop ancestors. In contrast the monophyletic story of endoferal weedy rye has been shown to have undergone both rapid evolutionary divergence from its progenitor as well as regional evolutionary diversification in considerably less than a century. We conclude with the curious case of California wild radish, an exoferal derivative of two species that spontaneously hybridize throughout the world; interestingly, that hybridization has yielded a problematic lineage in only one region.Weedy rice in China, the United States, and Bhutan Native to Asia, cultivated rice is the world’s most important food crop. Weedy rice , also known as ‘red rice’, has been an important weed of cultivated rice worldwide for hundreds of years . Vegetatively, weedy rice is a crop mimic , but its infructescence shatters, and its seeds typically exhibit some dormancy. When it co-occurs with rice, the crop suffers depressed yields, and, when co-harvested, the seeds of the weed degrade the quality of the harvested grain. Because it is the same species as cultivated rice, with similar morphology and physiology, it is very difficult to control by both weeding and chemical means. The evolutionary origin of weedy rice has been controversial. Its putative ancestry includes various hypotheses: that is a wild relative of rice that has evolved crop mimicry, that it is descended directly from cultivated rice, or that it is an exoferal lineage descended from hybrids between a wild taxon and cultivated rice . Three recent genetic studies of weedy rice have addressed its evolutionary origins. After decades of successful suppression, in the last decade weedy rice has emerged as a problem in the rice fields of certain regions of China . Motivated by the resurgence of this pest, Cao et al. compared 20 DNA based SSR markers from 30 populations of weedy rice collected from China’s Liaoning province with those of wild O. rufipogon as well as selected rice varieties from the two major cultivar groups, japonica and indica. Statistical analysis of the genetic data revealed the local Liaoning cultivar clustered within the array of weedy rice populations. Another major Chinese japonica cultivar showed much less affinity. The wild O. rufipogon and domesticated indica types were even more distantly related from the Liaoning weeds. The authors conclude ‘weedy rice populations from Liaoning most probably originated from Liaoning rice varieties by mutation and intervarietal hybrids’. We agree that an intertaxon hybrid origin for Liaoning weedy populations is unlikely; if hybridization had occurred, it is likely that some O. rufipogon alleles would have been retained in the weedy lineages in the short time that they have been problematic. Weedy rice has been a problematic weed of rice in the southeastern United States for well over a century . To identify the origins of this weed Londo and Schaal took a similar approach to Cao et al. , genetically analyzing 29 different United States weedy rice accessions from six different states to ‘cover the entire range of US rice culture’. For comparison, they chose 113 accessions representing a variety of indica and japonica cultivars, O. rufipogon, and other wild relatives. They used data from both sequencing a nuclear pseudo-gene and 21 DNA-based microsatellite loci.