What increases genetic variation when animals move from one population to another?

Migration and Gene Flow

Migration can change allele frequency by the process ofgene flow, defined as the slow diffusion of genes across a barrier. Gene flow usually involves a large population and a gradual change in gene frequencies. The genes of migrant populations with their own characteristic allele frequencies are gradually merged into the gene pool of the population into which they have migrated, a process referred to asgenetic admixture. The termmigration is used here in the broad sense of crossing a reproductive barrier, which may be racial, ethnic, or cultural and not necessarily geographical and requiring physical movement from one region to another. Some examples of admixture reflect well-known and well-documented events in human history (e.g., the African diaspora from the 15th to the 19th century), whereas others can only be inferred from the genomic study of variation in ancient DNA samples (seeBox).

Returning to the example of the 32-bp deletion allele of theCCR5 cytokine receptor gene, ΔCCR5, the frequency of this allele has been studied in many populations all over the world. The frequency of the ΔCCR5 allele is highest, up to 18%, in parts of northwestern Europe and then declines along a gradient into eastern and southern Europe, falling to a few percent in the Middle East and the Indian subcontinent. The ΔCCR5 allele is virtually absent from Africa and the Far East. The best interpretation of the current geographical distribution of the ΔCCR5 allele is that the mutation originated in northern Europe and then underwent both positive selection and gene flow over long distances (Fig. 9-1).

Ancient Migrations and Gene Flow

A fascinating example of gene flow during human prehistory comes from the sequencing of DNA samples obtained from the bones of three Neanderthals who died approximately 38,000 years ago in Europe. The most recent common ancestors of Neanderthals andHomo sapiens lived in Africa over 200,000 years ago, well before the migration of Neanderthals out of Africa to settle in Europe and the Middle East. An analysis of the sequence of Neanderthal DNA revealed that approximately 1% to 4% of the DNA of modern Europeans and Asians, but not of Africans, matches Neanderthal DNA. A variety of statistical techniques indicate that the introduction of Neanderthal DNA likely occurred approximately 50,000 years ago, well after the migration of modern humans out of Africa into Europe and beyond, which explains why traces of the Neanderthal genome are not present in modern Africans.

The analysis of individual Neanderthal genomes and their comparison to genomes of modern human populations promises to provide clues about characteristic differences between these groups, as well as about the frequency of possible disease genes or alleles that were more or less common in these ancient populations compared to different modern human populations.

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.

Gene Flow (Migration)

If new alleles are introduced into a population through migration and intermarriage, a change will occur in the relevant allele frequencies. This slow diffusion of alleles across racial or geographical boundaries is known as gene flow. The most widely quoted example is the gradient shown by the incidence of the B blood group allele throughout the world (Fig. 7.4), which is thought to have originated in Asia and spread slowly westward from admixture through invasion.

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.

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.

System of Mating and Gene Flow

Gene flow not only involves the dispersal of individuals across space but also the successful breeding of these individuals in their new locations. The local system of mating in the deme into which an individual migrates can affect the chances of breeding in the new deme, and hence the amount and pattern of gene flow. In particular, systems of mating that favor mating with relatives (inbreeding) or assortative mating tend to diminish gene flow, whereas disassortative mating or avoidance of inbreeding tend to augment gene flow.

Even nongenetic traits that influence mating and that are correlated with immigrant status can affect gene flow. For example, the Makiritare and Yanomama Indians lived contiguously in South America since at least 1875, but with little evidence for interbreeding (Chagnon et al., 1970), apparently due to cultural differences. As a consequence, most villages of these two adjacent tribes had significant genetic differentiation at many loci, including alleles in the Makiritare that are not present in the Yanomama gene pool. However, cultural environments change, and one major change was contact with European settlements. The Makiritare, a “river” people, first made contact with Europeans and acquired steel tools. The Yanomama, being a “foot” people and more in the interior, did not have contact with non-Native Americans until the 1950s. Hence, the Yanomama depended upon the Makiritare for steel tools for many decades. The Makiritare demanded sexual access to Yanomama women in exchange for the tools, siring many children who were raised as Yanomama, but effectively causing an asymmetric and gender-biased cultural disassortative mating. This also caused much animosity. One group of Yanomama (Borabuk) eventually moved away from the Makiritare. Sometime around 1930, the Borabuk Yanomama encountered a group of Makiritare. They ambushed the Makiritare, killing the men and abducting the Makiritare women. These women had low social status, and high-status Yanomama men sired an average of 7.3 children per captive Makiritare woman as compared with 3.8 children per Yanomama woman. This was gender-biased disassortative mating by social status. Because of this history, there were effectively two generations in which most offspring in the Borabuk Yanomama were actually Yanomama/Makiritare hybrids. This extreme gene flow between Yanomama and Makiritare, although not based upon any genetic traits, has lead to the current Borabuk Yanomama being genetically similar to the Makiritare, although culturally they are still Yanomama (Chagnon et al., 1970).

Assortative and disassortative systems of mating based on a phenotype that is inherited can cause locus-specific asymmetries in the amount of gene flow. For example, human populations often show assortative mating by skin color (Banerjee, 1985; Hulse, 1967; Vandenberg, 1972). As will be discussed in more detail later in this chapter, there has been much gene flow between European Americans and African-Americans in the United States. Lao et al. (2010) reported that the allele frequency differences have converged less (see Eq. 6.4) at the skin color gene SLC45A2 that influences skin pigmentation than for most loci. Consequently, the interaction of dispersal with system of mating can differentially affect specific loci depending upon whether or not a locus plays a role in influencing the system of mating.

Although dispersal is necessary for gene flow in humans, dispersal and gene flow are not the same. The system of mating can either amplify or diminish the amount of gene flow for a given amount of dispersal and can also induce asymmetries in the direction of gene flow and gender biases.

Gene Flow

Gene flow refers to the pollen-driven movement of trans- genes from a virus-resistant transgenic plant into a nontransgenic compatible recipient plant, for example, a wild relative. Hybrids resulting from gene flow can acquire and express virus-derived transgenes, and become resistant to the corresponding viruses. Subsequently, plants acquiring viral resistance traits can have a competitive advantage, exhibit increased fitness, and eventually become more invasive, maybe as noxious weeds. Movement of viral transgene constructs through pollen flow has been documented from virus-resistant transgenic squash into a wild squash relative under experimental field conditions. Hybrids between transgenic and wild squash exhibited increased fitness under conditions of intense disease pressure. In contrast, under conditions of low disease pressure, no difference was observed between hybrids and wild squash in terms of growth and reproductive potential. Since viruses do not limit the size and dynamics of wild squash populations in natural habitats, it is anticipated that gene flow with virus-resistant transgenic squash will be of limited significance. It remains to be seen if increased fitness will provide hybrids with a competitive edge that could eventually lead to enhanced weediness. Altogether, compelling evidence suggest that gene flow with virus-resistant transgenic squash should not be perceived more risky than the equivalent situation with virus-resistant conventional squash.

Gene flow can also occur from a virus-resistant transgenic plant into a compatible conventional plant. Although of negligible biological impact, this phenomenon can be essential for economical reasons such as organic production and export to countries that have not deregulated transgenic crops. Worth noting is the fact that the coexistence of transgenic and conventional papaya in spatiotemporal proximity is a reality in Hawaii.

10.5.1 Gene Flow and the Flow of Migrants

Gene flow measurement provides indirect information on the level of migration among subpopulations. Lack of gene flow is a valid information since in that circumstance (genetic divergence) migrants are highly unlikely. Less valid information is the similarity of gene frequencies, 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 on the evolutionary rate of the genetic marker.170 Additional problems with genetic markers are that they are relatively costly and they need appropriate infrastructures. Genetic markers often remain inside research laboratories and have not yet found their way into routine medical entomology.