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Gene Flow in Applied Evolutionary Biology Evolutionary Applications ISSN 1752-4571 EDITORIAL When gene flow really matters: gene flow in applied evolutionary biology species has had its benefits. The evolution of highland Introduction maize (Zea mays ssp. mays) landraces was the result of In the last half century, gene flow has moved from relative introgression from the wild Z. m. ssp. mexicana (Hufford obscurity to a well-recognized component of evolution. et al. 2013). Gene flow, the successful transfer of alleles from one popu- But gene flow involving domesticated species is not uni- lation to another, is now known to vary considerably versally beneficial. Pollen contamination from conspecifics among species, populations, and individuals as well as over and congeners growing within cross-pollination distance time. It frequently occurs at rates sufficient to play an can frustrate progress under artificial selection as well as important evolutionary role for populations of both ani- jeopardize the genetic purity of seed multiplication pro- mals and plants (Ellstrand 2014; Yakimowski and Rieseberg grams (e.g. Kelly and George 1998). Spontaneous gene flow 2014; Arnold 2015). into or out of domesticated populations sometimes gives Gene flow does not automatically come to mind in the rise to new invasive and weedy lineages (Ellstrand et al. context of evolutionary applications. When the senior 2010). The rise of Africanized bees in the New World may author shared the idea of a Special Issue on Gene Flow in be the best known example (Winston 1992). Another Applied Evolution with a colleague, she asked, “What else example is the case of the rise of herbicide-resistant weedy is there besides crop breeding?” Considerably more, as we rice in Brazil, reviewed in this issue (Merotto et al. 2016). shall soon see. A new herbicide-resistant cultivar of cultivated rice had Gene flow is important in a remarkable variety of applied been introduced to facilitate the control of the conspecific situations. This Special Issue presents some representative weed. A local economic boom ensued as yields increased. points in the galaxy of applied topics in which gene flow But the combination of introgression of the resistance allele plays a key role. The number of possible topics precludes into the weed and strong selection by the herbicide lead to an exhaustive treatment. Likewise, while we acknowledge the dramatic evolutionary spread of weed populations that non-sexual gene flow (horizontal transfer) has consid- bearing the allele for herbicide resistance, resulting in the erable applied and evolutionary significance in prokaryotes reversal of economic fortunes. In extreme cases, the farmers and eukaryotes (e.g. Koonin et al. 2001; Richardson and were compelled to abandon their land. Palmer 2007; Arnold 2015), the topic is so large, we deem The foregoing scenario involving a traditionally bred it worthy of separate treatment. crop represents one of the primary concerns associated with the release of transgenic crops (Ellstrand 2001): that is, the delivery of transgenes into free-living populations When gene flow really matters via gene flow might result in the evolution of new or more Gene flow involving domesticated species problematic weeds or invasives. It is not unusual for spon- The recognition of gene flow’s magnitude and variation taneous gene flow from crops to their wild or weedy rela- has led to increased attention to gene flow in applied evo- tives to result in introgression (Ellstrand et al. 2013). But lutionary biology. As noted above, breeders have long been whether or not those alleles will persist and spread also acutely aware of gene flow. Intentional anthropogenic gene depends on the relative fitness of free-living plants that bear flow has long been practiced by breeders to deliver desir- those alleles versus those that do not. Relevant multigener- able traits to domesticated species via wide crosses followed ational field experiments involving a variety of environ- by repeated backcrossing (e.g. Stalker 1980). But long ments remain few. before humans intentionally bred plants, spontaneous gene One such study is presented in this Special Issue. Xia flow played a role in plant improvement. A few thousand et al. (2016) measured the fitness effects of cultivated rice years ago, spontaneous interspecific hybridization gave rise insect resistance transgenes that had been introgressed into to first durum wheat and then bread wheat (Feldman et al. various weedy rice lineages. The relative fitness effect of the 1995). Likewise, lager beer yeast is the result of sponta- transgene varied with both environment (level of insect neous interspecific hybridization and of a similar age infestation) and genotype (genetic background of the dif- (Hebly et al. 2015). Even natural hybridization within ferent lineages). Correspondingly, the Special Issue includes © 2016 The Authors. Evolutionary Applications published by John Wiley & Sons Ltd. This is an open access article under the terms of the Creative 833 Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. Editorial a review of field studies of the fitness effects of crop trans- Gene flow and conservation genes with wild or weedy ancestors (Lu et al. 2016). The review reveals that the relative fitness of lineages that are The rise of conservation genetics in the 1980s started the result of gene flow between a transgenic crop and wild/ with a focus on fragmentation and small populations, weedy relative cannot easily be predicted a priori. The pres- featuring the hazards associated with drift, inbreeding, ence of transgenes sometimes correlates with increased rel- and lack of variation in the face of environmental chal- ative fitness, decreased relative fitness, or no change in lenges (Schonewald-Cox et al. 1983). Early on, gene flow relative fitness. Likewise, enough studies have accumulated was seen largely as a benefit for populations at risk of to demonstrate that genetic background and environment extinction as an agent that would reverse those hazards can sometimes play a key role in determining the direction (Lacy 1987). and magnitude of transgene fitness effects. The intentional introduction of new genetic diversity for Two decades after the commercial release of genetically the purposes of sustaining a population is called “genetic engineered crops, gene flow has enabled crop transgenes to rescue” (Tallmon et al. 2004). For small, inbred popula- move into and apparently persist in free-living populations. tions, outcrossing with conspecific populations with similar The known cases are relatively few and mostly involve feral environmental adaptations typically does lead to an canola (Ellstrand 2012). Thus far, the economic and envi- increase in fitness. Indeed, in a recent meta-analysis, posi- ronmental impacts of transgenes in free-living populations tive fitness effects were report in 93% of such cases (Frank- have been nil or, at worst, mild. As noted above, gene flow ham 2015). A caveat is that Frankham (2015) focused on between traditionally improved domesticates and their wild systems that are at low risk for outbreeding depression, and relatives sometimes results in lineages that are not so his conclusions may not apply to cases where gene flow benign. occurs between genetically and/or ecologically divergent populations. Of course, the addition of genetic diversity almost Gene flow and the evolution of novel weeds and invasives always includes the introduction of new individuals. The evolution of novel weeds and invasives need not Thus, genetic and demographic relief can be confounded. involve domesticates at all. Natural gene flow and subse- In this Special Issue, Fitzpatrick et al. (2016) estimate the quent admixture involving only non-domesticated taxa are relative contributions of genetic and demographic factors known to have preceded the evolution of dozens of new to the rescue of two wild guppy populations from Trini- weedy and invasive lineages (Schierenbeck and Ellstrand dad. Using molecular markers to distinguish between 2009). Examples include plants, animals, and microorgan- native and immigrant genotypes, and to determine the isms. Recently, an increasing number of studies have parentage of offspring, they were able to show that the revealed that even within-species admixture appears to demographic contribution of the new immigrants was have played a role in the evolution of many invasive lin- indeed substantial. However, hybrid genotypes were eages (Rius and Darling 2014). In that case, admixture major contributors to population expansion as well, depends on multiple introductions (Bock et al. 2015). possibly due to heterosis. Thus, both genetic and demo- Likewise, a small, but growing, number of examples of graphic factors play an important role in the evolution- invasives that evolved from intertaxon hybridization have ary rescue of these populations. been shown to be the result of multiple, independent As conservation genetics began to mature, gene flow was hybridization events. no longer perceived solely as a panacea for the ills of small One such example is in this Special Issue. The tumble- populations. Significant genomic or eco-genetic differences weed, Salsola ryanii, evolved in California as recently as a between source and recipient populations can result in a few decades ago and is certainly no more than a century fitness drop in interpopulation hybrids, often deemed old. An allohexaploid derivative of hybridization between “outbreeding depression.” If differences
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