What is the movement of alleles from the first population to the second population an example of?

Dispersal

Although gene flow is not synonymous with dispersal, it is certainly true that long-distance dispersal provides the opportunity for long-distance gene flow, and hence for high levels of gene flow among populations. The larvae of some marine mollusks have been documented to be carried by equatorial currents from the coast of Africa to the Caribbean Sea, and we would expect those species to have high levels of gene flow among populations in Africa or in the Caribbean. On the other hand, some marine mollusks brood their young, or attach egg cases to the substrate, severely limiting the opportunity for dispersal, and restricting gene flow. Species that are philopatric with respect to breeding sites, such as salamanders and some species of birds that return to breed where they were born, are characterized by very low gene flow and high levels of genetic differentiation among populations.

2.3.3 Gene Flow and Introduction of Genetic Diversity

Gene flow is also called gene migration. Gene flow is the transfer of genetic material from one population to another. Gene flow can take place between two populations of the same species through migration, and is mediated by reproduction and vertical gene transfer from parent to offspring. Alternatively, gene flow can take place between two different species through horizontal gene transfer (HGT, also known as lateral gene transfer), such as gene transfer from bacteria or viruses to a higher organism, or gene transfer from an endosymbiont to the host. HGT is discussed in detail later in this chapter. Gene flow within a population can increase the genetic variation of the population, whereas gene flow between genetically distant populations can reduce the genetic difference between the populations. Because gene flow can be facilitated by physical proximity of the populations, gene flow can be restricted by physical barriers separating the populations. Incompatible reproductive behaviors between the individuals of the populations also prevent gene flow.

Gene and Genotype Flow among Plant Pathogens

Gene flow is the process by which certain alleles (genes) move from one population to another geographically separated population. In plant pathology, gene flow is very important because it deals with the movement of virulent mutant alleles among different field populations. High gene flow in a pathogen increases the size of the population and of the geographical area in which its genetic material occurs. Therefore, pathogens that show a high level of gene flow generally have greater genetic diversity than pathogens that show a low level of gene flow. In pathogens reproducing only asexually, in which no recombination occurs, entire genotypes can be transferred from one population to another. This is known as genotype flow. Pathogens that produce hardy spores or other propagules, such as rust and powdery mildew fungi, that can spread over long distances, can distribute their genomes over large areas, sometimes encompassing entire continents. However, soil-borne fungi and nematodes move slowly and are present in small areas and their level of genetic flow is limited. With all types of pathogens, however, their gene flow can be affected significantly by human agricultural practices and by intercontinental travel and commerce. In general, pathogens with a high level of gene flow or genotype flow are much more effective and pose a greater threat to agriculture than pathogens with a low level of gene flow. Also, because asexual spores and propagules contain an already well-adapted and selected set of alleles, such propagules, through their geno-type flow, pose a greater threat in enlarging the area of their adaptation than sexual propagules through their gene flow.

The frequency of alleles of importance in a population is affected by gene flow from other populations. Its magnitude depends on the number of incoming outside individuals into the population compared to the size of the population, as well as the number of different alleles brought into the population by outside individuals. Usually, allele frequencies in small populations adjacent to large ones are influenced strongly by gene flow than under any different conditions. Gene flow between distant populations is generally sporadic unless it is facilitated by intervening populations that act as stepping stones for the pathogen. The effect of gene flow is to reduce genetic differences between populations, thereby preventing or delaying the evolution of the populations in different geographical areas into separate species of the pathogen.

Gene Flow and the Flow of Migrants

Gene flow measurement provides indirect information on the level of migration among subpopulations. However, this information is of unequal value depending on its output, either “lack of gene flow” or “complete gene flow.” Lack of gene flow is valid information since in that circumstance (genetic divergence) migrants are highly unlikely. Less valid information is the case of complete gene flow, since no one can affirm that such (lack of) genetic structure is a reflection of the current level of migration. How contemporaneous or recent it depends on the effective size of the populations under study and the evolutionary rate of the genetic marker (McKay and Latta, 2002). Additional problems with genetic markers are that they are relatively costly and they need appropriate infrastructures. As an unfortunate consequence, genetic markers often remain inside research laboratories and have not yet found their way into routine medical entomology.

III.F. Gene Flow

Gene flow is a fundamental agent of evolution based on the dispersal of genes between populations of a species. It involves the active or passive movement of individual plants, animals, gametes, or seeds. Gene flow involves not just dispersal but also the successful establishment of the immigrant genotypes in the new population. Gene flow is often confusingly referred to as migration, but the latter term is best reserved to describe dispersal behaviors involving a seasonal or longer term round-trip. Gene flow tends to homogenize linked populations and lack of gene flow permits interpopulation differentiation. It is of interest to geneticists and managers in that to conserve a population one needs to establish the historical patterns and rates of gene flow. This is typically estimated from allele frequency data and reported in terms of the number of “migrants” per generation. In theory, one migrant per generation between two populations will ensure that they remain genetically homogeneous. Inbreeding depression can be ameliorated by the artificial translocation of one reproducing migrant per generation between populations.

Gene flow is often gender biased and limited to certain phases of the life cycle. It may be accelerated under certain climatic conditions that occur at frequencies of many years or at irregular intervals many years apart. Interspecific gene flow results in introgressive hybridization (discussed previously). The translocation of individual organisms results in gene flow if they reproduce at the release site. In the future, genetically depauperate populations will be enhanced by translocation of individuals from more secure areas. Unfortunately, such genetic enhancement carries risks associated with the introduction of pathogens that could harm the target population or completely unrelated species. Furthermore, the introduction of individuals from genetically well-differentiated source populations may result in outbreeding depression in the threatened population of conservation concern (discussed previously). Gene flow can thus erode the genetic basis of adaptation to local conditions.

If previously continuous populations become fragmented, historical patterns of dispersal and gene flow may be disrupted with potentially serious consequences for population viability. For example, if young female chimpanzees can no longer emigrate from their natal social group because of habitat destruction in the surrounding countryside, their isolated natal population will experience increased inbreeding.

7.1.1 Gene Flow

Gene flow is a natural process that occurs among sexually compatible individuals in which cross-pollination can lead to the production of viable seeds. Gene flow between individuals within and among populations occurs via pollen only when they have concurrent geography, overlapping flowering times, and they share common pollinators. Gene flow in GM crops is not desired because there are possibilities of genes from GM crops moving into their wild relatives in conventional or organic crops. In some instances, large economic losses have occurred because of gene flow, leading to zero tolerances for admixtures, none of which were a food or environmental safety concern. Nonetheless, to avoid market impacts and associated economic losses, a comprehensive understanding and control of gene flow as well as realistic thresholds are required for consistent marketing of agricultural commodities.

Gene flow among crop plants has been reviewed from various angles (Kwit et al., 2011; Ding et al., 2014) and compiled information is available on gene flow to wild relatives in the top 25 crops (Gealy et al., 2007). Sexually compatible wild relatives exist for cassava, cotton, grape, oats, oilseed rape, sorghum, sugarcane, sunflower, wheat, and most of the commonly grown forest trees. Examples of gene flow from transgenics to wild or weedy relatives have been reported in at least 13 species. Although hybridization is possible in these species, introgression was studied only in brassica, wheat, and creeping bent grass. In those cases, none of the weedy relatives indicated signs of invasiveness or selective advantage because of herbicide or insect resistance (Kwit et al., 2011). Gene flow studies in crops have been reviewed by Chandler and Dunwell (2008) and trees by Dick et al. (2008; see case studies for recent studies).

Gene Flow and Population Structure

Gene flow is the process acting on and creating genetic sub-populations. The flows occur over landscapes and amongst populations that are distributed in space with varying distances of separation. Whether space is simple or complex in a model, we need to carefully define gene flow and population structure and deal with both concepts simultaneously. The genetic structure of the population in a landscape is determined by gene flow, and the movement of genotypes and genes is dependent on the spatial structure of the population.

Background on the population-genetic issues related to gene flow can be obtained from several publications (Hedrick, 2006). Mallet (2001) provides one of the best recent overviews of gene flow. He clarifies a number of issues that often confuse non-experts, emphasizing the actual movement of genes and genotypes in his analysis. Felsenstein (1976) reviews research concerning models of island populations and dispersal. This traditional work in population genetics still has relevance to current problems regarding patches of transgenic insecticidal crops and refuges of conventional crops. In particular, Felsenstein (1976) summarizes the relatively old studies by stating that the alleles found in island populations will depend on the amount of dispersal amongst the islands, with threshold levels of dispersal possibly determining the final outcome. Several authors have studied gene flow in heterogeneous landscapes (Caprio and Tabashnik, 1992; Caprio, 2001; Ives and Andow 2002; Sisterson et al., 2005).

Care must be taken when using the term gene flow or claiming some consequence of gene flow for IRM. Gene flow depends on dispersal. To understand these complex processes, several factors must be identified for each resistance gene. First, does the dispersal occur before or after mating, or both? Second, do males and females have different dispersal rates and behaviors? Third, is gene flow unidirectional or multi-directional? If flow occurs in several directions, such as to and from a particular crop or refuge, are the flows equal or unequal? Are they equal in terms of proportion of gene or insect population or in terms of numbers of alleles or insects? Fourth, is dispersal a constant over time and space or does it interact with (a) other processes, (b) insect density, or (c) environmental conditions? Thus, when someone claims to know how gene flow affects evolution of resistance, be prepared to ask a series of questions.

Gene Flow under Climate Change

Gene flow is a natural biological process that occurs to some degree in all flowering plants; four steps can be delineated in the process: (i) gene flow through pollen or seed, (ii) spontaneous hybridization, (iii) hybrid behavior, fitness cost due to hybridization and introgression, and (iv) fitness benefits due to transgenes. Each step can potentially be impacted by environmental and climatic conditions and stresses. Pollen and grain development are the most sensitive stages for temperature stress (Singh et al., 2012). Therefore, pollen-mediated gene flow and subsequent hybridization and grain development can be impacted by GCC. In addition, shape and composition of a cropping system can impact spatiotemporal gene flow through seed bank dynamics (Liu et al., 2013). Pollen-mediated gene flow between crops, CWR or weeds, can introduce new alleles into oilseed crops with the probability of introgression depending on the degree to which the new alleles alter fitness and therefore are selected for in nature. A cultivated oilseed crop is more likely to hybridize with closely related wild species having a similar ploidy level, genome, and chromosome-pairing ability (De Jong and Rong, 2013).

Oilseed crop biology will determine seed fate (i.e., dormancy, germination, or mortality) and can influence the success of allele introgression. For example, duration of the flowering period of an oilseed crop, especially crops with indeterminate flowering habits with the possibility of viable flowers being present at harvest, determines potential flowering synchronicity with its wild relatives. Additionally, GCC stress components will determine how successful the introgression will be, and what role hybrids will play in metapopulation dynamics (Warwick and Martin, 2013). Oilseed crops differ as to their genetic base, phylogenetic origin, mode of pollination, outcrossing rate, and the rate of gene flow. Compared with Linum usitatissimum L., Arachis hypogaea, for example, has a narrow genetic base due to its monophylogenetic origin, is selfpollinated, and virtually lacks gene flow. Gene flow and hybridization of transgenic L. usitatissimum L. or B. napus, for example, with many wild relatives depend on species sympatric distribution, concurrent flowering, ploidy level, sexual compatibility, and potentially on environmental conditions. However, no gene flow has been verified yet, for example, from transgenic B. juncea (for herbicide resistance) into the weedy Sinapis arvensis (Warwick and Martin, 2013). Nevertheless, in this and similar cases of gene flow, the transgene may persist, as subsequent generations populations are formed that have selfing capacity, normal fertility, and dormancy that may contribute to persistence of the transgene and the herbicide resistance trait in nature.

Gene flow, in the case of spatiotemporal coexistence of genetically modified and non genetically modified oilseed crops (e.g., B. napus), may have far-reaching effects on survival, dormancy, emergence, and seed bank evolution (Haile et al., 2014), and in the metapopulation dynamics role of natural hybrids (De Jong and Rong, 2013). Feral populations of B. napus, due to siliqua shattering, may persist for up to 8 years without human intervention (Gepts, 2002) with potentially increasing intensity of gene flow. Gene flow from transgenic plants to wild relatives may cause wild plants to acquire traits that improve or impair their fitness in natural habitats. There is a rising concern over crop-to-crop gene flow in Linum usitatissimum under field conditions. Gene flow from high α-linolenic acid cultivars to low α-linolenic acid cultivars under the changing climate of western Canada has economic repercussions. Therefore, a better understanding of crop-to-crop or crop-to-weed gene flow is essential for ecological risk assessment (Gressel, 2014). A key environmental risk of transgenic oilseed crops is potential gene flow into feral populations or to wild relatives of the crop and the emergence of invasive plants or the loss of already endangered wild genetic diversity.

Gene Flow Can Promote Local Adaptation

Gene flow need not be an antagonist to adaptation. Most importantly, it spreads universally favored mutations across a species range (for a review see Morjan and Rieseberg, 2004). It can also aid local adaptation by supplying new alleles to populations with limited genetic variance. This can facilitate adaptation at the edge of a species range (see Geber, 2011 and associated papers) or after a drastic reduction in population size. The coevolution between parasites and hosts represents another evolutionary process in constant need of new genetic variation.

The theoretical prediction that gene flow can facilitate local adaptation in such systems (Gandon, 2002) has been experimentally tested with bacterial hosts and bacteriophage “parasitoids.” Experimental evolution in microbes allows for the study of large, replicated populations over many generations and for the direct comparisons of genotypes across time (i.e., from frozen stocks). In the present context, it also enables the experimenter to control a suite of key parameters that would be difficult to measure let alone manipulate in nature. Compared to a set-up without gene flow, regular genetic exchange between replicate microcosms of bacteria and phage increased both the overall occurrence and the spatio-temporal variability of local adaptation in the phage (Forde et al., 2004). The latter observation might explain why snapshots of unmanipulated host–parasite systems in nature give overall inconsistent results with regard to local adaptation. In another study (Morgan et al., 2005), host and parasitoid gene flow rates were manipulated independently (either host or parasitoid or no gene flow). As before, parasitoid gene flow led to increased local adaptation in parasitoids. In addition, there was evidence at the end of the experiment that parasitoid gene flow had increased parasitoid adaptation to nonlocal hosts, which could reflect the spread of universally favored alleles. Interestingly, host gene flow had no effect on the level of local adaptation in the host.

IV.A. Direct and Indirect Measures of Gene Flow

Gene flow clearly plays a central role in the dynamics of ecological variants in heterogeneous environments. Its role has been the matter of considerable controversy in the past. Does wide ranging gene flow impose limits on intraspecific differentiation or is gene flow on the contrary so limited that populations of a species behave as nearly independent evolutionary units? Based on the available evidence, the latter view is closer to the truth. Nevertheless, it is difficult to predict the potential for local adaptation and differentiation for any given species. Reliable estimates of gene flow are thus highly desirable. They might be obtained by monitoring the movement of marked individuals. However, such direct estimates typically give an underestimate of gene flow. Long distance dispersers will often be missed, yet they play an important role in the spread of genes. Mark-recapture studies provide a snapshot of dispersal whereas a longer-term average is required for evolutionary inferences. On the other hand, not all observed movement necessarily leads to gene flow. For example, immigrants might be less successful than residents in the competition for territories. Much effort has therefore been devoted to the developments of indirect measures of gene flow that can provide a suitably averaged estimate. Most of these methods are based on the spatial distribution of neutral genetic markers.

Consider again the island model: a large number of demes, each of constant size N, are connected by gene flow at a rate m via a common pool of migrants. The overall frequency of a certain selectively neutral allele in the population as a whole, and consequently in the migrant pool, is p¯. Genetic drift within demes produces variance in p across demes as a function of local population size. Without gene flow, this process would inevitably lead to the random fixation of one or the other allele in each deme. With gene flow there is an equilibrium amount of differentiation: the divergence among demes due to drift is balanced by the homogenizing effect of gene flow such that the variance in p, Vp, is constant. For a locus with two alleles, Sewall Wright defined the standardized variance in allele frequency as Fst = Vp/p¯(1− p¯) and showed for the island model that

Fst≈11+4Nm

The degree of differentiation among demes in the island model thus depends on the number of migrants per deme per generation. Consider a given combination of N and m. An increase in N reduces random drift such that a smaller migration rate suffices to keep Vp constant. The two forces exactly balance each other. The analysis of the island model shows that only a small amount of gene flow is enough to maintain neutral genetic variability within demes. The threshold number of migrants below which there is a tendency for demes to fix by chance one or the other allele is Nm = 0.5, which is equivalent to one migrant every other generation or an Fst-value of 0.33.