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Keywords:

  • disease;
  • domestication;
  • introgression;
  • natural hybridization;
  • pests

Abstract

  1. Top of page
  2. Abstract
  3. Introduction
  4. Introgressive hybridization and the evolution of domesticated plants
  5. Introgressive hybridization and the development of domesticated animals
  6. Natural hybridization and the evolution of pathogens, pests and vectors
  7. Concluding remarks
  8. Acknowledgements
  9. References

The role of natural hybridization in the evolutionary history of numerous species is well recognized. The impact of introgressive hybridization and hybrid speciation has been documented especially in plant and animal assemblages. However, there remain certain areas of investigation for which natural hybridization and its consequences remain under-studied and under-appreciated. One such area involves the evolution of organisms that positively or negatively affect human populations. In this review, I highlight exemplars of how natural hybridization has contributed to the evolution of (i) domesticated plants and animals; (ii) pests; (iii) human disease vectors; and (iv) human pathogens. I focus on the effects from genetic exchange that may lead to the acquisition of novel phenotypes and thus increase the beneficial or detrimental (to human populations) aspects of the various taxa.


Introduction

  1. Top of page
  2. Abstract
  3. Introduction
  4. Introgressive hybridization and the evolution of domesticated plants
  5. Introgressive hybridization and the development of domesticated animals
  6. Natural hybridization and the evolution of pathogens, pests and vectors
  7. Concluding remarks
  8. Acknowledgements
  9. References

In his classic work English Literature in the Sixteenth Century, C.S. Lewis stated the following regarding the impact of the sciences on the humanities: ‘Perhaps every new learning makes room for itself by creating a new ignorance … Man's power of attention seems to be limited; one nail drives out another’ (Lewis 1954). However, the displacement and loss of an appreciation for the explanatory power of a conceptual framework also occurs within disciplines. For example, Lewis might just as well have been reflecting on the formation of a new series of paradigms during the neo-Darwinian synthesis — paradigms that have great explanatory power, but which also replaced (or led to the dismissal) of equally powerful and plausible conceptual frameworks. Yet, such replacements often reverse themselves; the ‘nail’ driven out can reappear when new data come to light. This is the case for a hypothesis concerning the evolutionary creativity of natural hybridization.

It can now be said that natural hybridization is once again considered to be of major evolutionary importance. This re-appreciation has gained momentum over the last two decades. During this time, numerous empirical studies have demonstrated both its effects across a wide taxonomic range and the variety of its creative results — including hybrid speciation, introgression and reinforcement of reproductive barriers. Although a few opponents to this viewpoint still exist (e.g. Schemske 2000), the mass of evidence continues to mount regarding the importance of this process in shaping the evolutionary trajectory of numerous animal and plant clades (e.g. Arnold 1992, 1997; Grant & Grant 1992, 2002; Dowling & DeMarais 1993; Howard 1993; Rieseberg 1997; Husband & Schemske 1998; Johnston et al. 2003; Rieseberg et al. 2003). However, some aspects of this process remain under-appreciated. One such aspect relates to the origin and evolution of organisms that affect human populations.

Natural hybridization has been defined as ‘Successful matings in nature between individuals from two populations, or groups of populations, that are distinguishable on the basis of one or more heritable characters’ (Arnold & Burke 2004; as adapted from Harrison 1990). In this review, I extend this definition to include gene flow between domesticated forms and their wild relatives or between different cultivars (plants or animals) that is not facilitated by artificial crosses (e.g. crosses between plant cultivars and wild populations via pollinator visitation rather than by human transfer of pollen). I also include within this conceptual framework horizontal transfer between different microorganisms resulting from genetic recombination. By extending the definition of natural hybridization in this way, I am able to demonstrate the important role played by recombination between divergent genomes in the origin of domesticated plants and animals, disease vectors, diseases and pest species.

The first topics discussed in this review illustrate the role played by natural hybridization in the evolutionary history of a class of organisms that benefit humans, i.e. domesticated plants and animals. I discuss the various outcomes of hybridization in which the wild relatives contribute to the gene pools of previously domesticated taxa. In particular, I highlight studies that have detected the effects of introgression on the genetic variation and evolutionary trajectory of cultivated plants and animals. In subsequent sections I discuss the role played by natural hybridization and introgression on the evolutionary development of organisms that have detrimental effects on human populations — plant pests and plant diseases that attack cultivars, vectors for human diseases, and human pathogens. As for the ‘beneficial’ organisms, I highlight how natural hybridization has helped mould the genetic architecture and evolutionary development of these ‘detrimental’ taxa.

Introgressive hybridization and the evolution of domesticated plants

  1. Top of page
  2. Abstract
  3. Introduction
  4. Introgressive hybridization and the evolution of domesticated plants
  5. Introgressive hybridization and the development of domesticated animals
  6. Natural hybridization and the evolution of pathogens, pests and vectors
  7. Concluding remarks
  8. Acknowledgements
  9. References

Significant primary data papers and reviews have been published concerning the effects of gene flow from crop plants into related wild forms. In particular, concerns over introgression from genetically modified crops into their wild relatives that promotes the evolution of invasiveness have been clearly elucidated (e.g. Ellstrand et al. 1999; Ellstrand & Schierenbeck 2000; Burke & Rieseberg 2003; Ellstrand 2003). In addition, it has been clearly demonstrated that numerous crop species are polyploid derivatives from hybridization events (e.g. Huang et al. 2002). Finally, hybridization between domesticated forms, mediated by their cultivation in close spatial proximity, has been implicated in the establishment of new cultivars (e.g. Santalla et al. 2002).

In contrast to previous emphases, I highlight the potential importance of natural introgression, following domestication, from wild species into their crop derivatives. In some instances, hybridization that leads to gene flow from wild taxa into their cultivated relatives may result in weedy forms (e.g. Coulibaly et al. 2002; Viard et al. 2002). These weedy derivatives may then act as reoccurring bridges for gene flow between the wild and domesticated populations. In other cases, gene flow is not clearly associated with the development of weedy derivatives (e.g. Toumi & Lumaret 1998). Regardless of the mechanism by which introgression occurs, the case studies discussed below indicate the possibility for it to result in adaptive changes that increase the number of habitats occupied by the cultivated form(s).

Maize and teosinte — introgression and landraces

Numerous, elegant analyses have appeared documenting the genetic and evolutionary development of the maize (Zea mays ssp. mays)/teosinte (e.g. Z. mays ssp. parviglumis and ssp. mexicana) complex (e.g. Doebley et al. 1997). These studies have addressed diverse hypotheses ranging from hybrid speciation (involving a third genus, Tripsacum; e.g. Talbert et al. 1990) to the molecular changes resulting in the morphological differentiation of maize (e.g. Doebley et al. 1995). More recently, an analysis was undertaken to test whether the diversity among the maize landraces reflected independent origins (Matsuoka et al. 2002). Results from this study indicated that all landraces likely arose from a single domestication event. In regard to the current topic, this investigation also detected post-domestication gene flow from teosinte (ssp. mexicana) into maize. At elevations where ssp. mexicana co-occurs with maize, 0.2–12% of the genomes of the landraces consist of teosinte DNA. In contrast, races of maize at lower elevations (where ssp. mexicana does not occur) had only 0.2–2% of their genomes made up of teosinte germplasm (Matsuoka et al. 2002). Furthermore, there was an even larger contribution of teosinte in the genomes of some higher elevation maize landraces leading to the conclusion that ‘… gene flow from ssp. mexicana may have contributed appreciably to some races of the Mexican highlands …’ (Matsuoka et al. 2002). Thus, wild [RIGHTWARDS ARROW] crop introgression has significantly affected the genetic architecture of these high-elevation landraces, and has possibly been the factor allowing their survival and maturation in these extreme settings.

Beets and soybeans — weeds, hybrid swarms and introgression

One outcome of introgression between wild and cultivated taxa is the production of ‘weedy’ (i.e. hybrid populations associated with the disturbed, agricultural settings) forms. This is the case for crops such as cowpea (Coulibaly et al. 2002), common bean (Papa & Gepts 2003) and beets (Desplanque et al. 1999; Viard et al. 2002). For some complexes the genetic bridge afforded by the weedy forms appears to have produced asymmetry in gene flow whereby introgression into wild populations is much greater than gene flow into the cultivar (e.g. Coulibaly et al. 2002; Papa & Gepts 2003). In other wild/cultivar assemblages, gene flow from the wild form, through weedy intermediates, into the cultivated form may affect greatly the genetic constitution of the cultivar. An example of this latter outcome has been detected for the sugar beet Beta vulgaris. Introgression among cultivated, wild and weedy forms has been detected on both macro- and microgeographical scales (Fig. 1; Desplanque et al. 1999; Viard et al. 2002). Indeed, an added taxonomic complexity involving the formation of ‘ruderal’ races has been found at the macrogeographical scale (Desplanque et al. 1999). Although most closely related to wild progenitors, the ruderal forms also possess the genetic signature of introgression from sugar beets (Desplanque et al. 1999). Thus, the weedy genotype bridge has facilitated both wild population to crop and crop to wild population gene flow.

image

Figure 1. Unrooted neighbour-joining phenogram illustrating the genetic relationships among ‘in-row’ and ‘out-row’ weeds in two cultivated Beta vulgaris (sugar beet) fields (i.e. Sainghin and Cantons). The in-row weeds are crop-wild hybrids and the out-row weeds are backcrossed crop-wild hybrids. The scale bar indicates the genetic distance (from Viard et al. 2002).

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Another genetically and evolutionarily significant result related to the genetic bridge concept occurs when wild by cultivar hybridization leads to the formation of a wide range of genotypes and phenotypes. Populations arising from natural hybridization that demonstrate this elevated level of variation are termed ‘hybrid swarms’. Grant (1981) defined hybrid swarms as populations consisting of ‘… a complex mixture of parental forms, F1 hybrids, backcross types, and segregation products.’Grant (1981) went on to explain that these populations exhibit ‘… a very high degree of individual variability.’Xu et al. (2002) suggested that the formation of new soybean cultivars (Glycine max) may have resulted from hybrid swarms between the wild progenitor, Glycine soja, and previously cultivated G. max populations. Conceptually, this hypothesis is similar to the observation of introgression through a weedy intermediate form. Furthermore, it is also hard to differentiate the process and outcome of hybrid swarm formation from the process leading to the various landraces of maize and other species (e.g. Matsuoka et al. 2002). However, the importance of the soybean example is reflected in the conclusion that from the extreme variation in the hybrid swarm, one might see the generation of a host of cultivar types (Xu et al. 2002). These novel forms could then, through crosses with the wild species, form new hybrid swarms leading to the evolution of the next generation of cultivars.

Introgressive hybridization and the development of domesticated animals

  1. Top of page
  2. Abstract
  3. Introduction
  4. Introgressive hybridization and the evolution of domesticated plants
  5. Introgressive hybridization and the development of domesticated animals
  6. Natural hybridization and the evolution of pathogens, pests and vectors
  7. Concluding remarks
  8. Acknowledgements
  9. References

As with crop development, the evolution of domesticated animal resources occurred in centralized geographical areas. In addition, the history of animal domestication often took place in multiple, rather than single centres of origin (e.g. MacHugh et al. 1997; Kijas & Andersson 2001; Luikart et al. 2001). Finally, having arisen in multiple regions, the domesticated forms were then brought into contact by human migration and trade (e.g. MacHugh et al. 1997; Kim et al. 1999; Vilàet al. 2001).

Along with breeding programmes, natural hybridization has played a pivotal role in shaping the genetic and evolutionary trajectories of domesticated animal species. This process has occurred between different domesticated races that have escaped or been released into the wild (e.g. Giuffra et al. 2000), and between wild progenitors and their domesticated derivatives (e.g. Vilàet al. 1997; Lau et al. 1998). The latter process is highlighted by the following quote from Luikart et al. (2001): ‘Diverse origins and repeated gene flow from wild stock have probably facilitated the development of the widely different and highly productive breeds we have today.’ Though these authors were reflecting upon the development of ‘walking larders’ (e.g. cattle, goats, sheep and water buffalo; MacHugh & Bradley 2001), the same conclusion is applicable to domesticated animals not used solely as food sources (e.g. dogs; Vilàet al. 1997).

Pigs and sheep: feral populations and hybridization as the basis of new domesticates and ‘wild’ species

Underlying genetic complexity is commonly discovered by studies of the evolution of domestic plants and animals. This complexity represents the footprints of evolution (natural and man-mediated) in the wild and domesticated populations. For example, the domestication of llama and alpaca involved multiple species, post-domestication hybridization, severe bottlenecks (due to the near extirpation of human populations through conquest) and line breeding (Kadwell et al. 2001). Findings from the analysis of llama and alpaca, and their progenitors (i.e. vicuña and guanaco), led Kadwell et al. (2001) to conclude that ‘Such complexity [in the evolution of domestic animals] is not without precedence … and requires detailed analysis and cautious interpretation.’ Domestication of sheep and pigs, like the North American camelids, has involved numerous stages and processes. One of the evolutionary stages I wish to highlight involves feral populations and hybridization as sources for (i) new domesticated forms and (ii) ‘wild’ species.

Two lineages of domestic swine, involving different subspecies of the wild boar (i.e. Sus scrofa), arose separately in Europe and Asia (Paszek et al. 1998; Giuffra et al. 2000). Subsequent to the European and Asian domestication events, the two forms were brought into contact in various parts of the world through human trade and migrations (Giuffra et al. 2000). One outcome of this contact was human-mediated hybridization and introgression, with the man-made hybrids forming the basis of major breeds of European pigs (Giuffra et al. 2000). However, human-mediated crosses between domestic animals were not the only avenues for the derivation of new domestic populations. In a survey of wild boar and domestic pig populations from Asia, Europe, Israel and the South Pacific, Giuffra et al. (2000) discovered a hybrid mitochondrial DNA (mtDNA) and nuclear genotype in the single, domesticated pig assayed from the Cook Islands. These authors argued that such hybridization was not surprising given the accidental or intentional release of pigs from Asian and European stocks by Polynesian and European explorers and settlers, respectively. The presence of hybrid genotypes in the Cook Islands would, however, indicate that natural hybridization in the feral populations was the final step in a domestic isolate [RIGHTWARDS ARROW] feral population [RIGHTWARDS ARROW] natural hybridization [RIGHTWARDS ARROW] domestic isolate cycle (Giuffra et al. 2000). It is likely that such cycles have continually impacted the genetic structure and evolutionary paths of domestic populations wherever there has been a history of feral populations originating from domestic animals from different geographical centres of origin.

A different cycle, but one also involving feral populations (and possibly their hybridization with domestic forms), has been hypothesized for wild and domestic sheep. As with most other domesticated animals, the culture of sheep from wild populations had multiple centres of origin located in Europe and Asia. In two studies, Hiendleder et al. (1998, 2002) described patterns of genotypic variation indicative of introgression between feral and domesticated forms and the subsequent formation of ‘wild’ taxa from these natural hybrid populations. In particular, results from both studies indicated a high degree of similarity between domestic sheep (Ovis aries) and wild sheep belonging to the European mouflon species, Ovis musimon (Fig. 2). Hiendleder et al. (1998) found that haplotypes in the mouflon samples were identical, or highly similar, to the European domestic sheep haplotypes. They concluded that the European mouflon may have originated from feral Neolithic sheep (a conclusion reiterated by Hiendleder et al. 2002). However, I would argue that the derivation of the mouflon populations might instead reflect subsequent, repeated bouts of natural hybridization with other feral populations of independent origin, or with domestic populations. Given the repeated opportunity for bi-directional introgression, the latter explanation would account for the high degree of genetic similarity between the mouflon and domestic sheep populations. Thus, the wild and domesticated forms would be expected to demonstrate the pattern discovered by Hiendleder et al. (1998, 2002), that of identical or nearly identical shared polymorphisms.

image

Figure 2. Unrooted consensus tree based upon mtDNA haplotypes identified in populations of wild and domesticated sheep. Sheep taxa included in the analysis were the argali (Ovis ammon nigrimontana and O. ammon collium), urial (O. vignei bochariensis), mouflon (O. musimon) and domesticated European (O. aries, a–i) and Asian (O. aries, j–n) forms. Bootstrap values that exceeded 50% are indicated on the appropriate branches (from Hiendleder et al. 1998).

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Reindeer, water buffalo and dogs: domestication and hybridization between progenitor and derivative

As with crop plants, domesticated animals often cross with their progenitors in areas of sympatry. The resulting gene exchange can lead to increased genetic similarity between progenitor and derivative and thus to an evolutionary web, rather than a diverging tree (Arnold 1997). One example of such a web of interactions is apparent for two forms of tundra caribou in southwestern Greenland. The native Rangifer tarandus groenlandicus and the semidomesticated, Rangifer tarandus tarandus, were brought into contact by human-mediated introduction of the latter (Jepsen et al. 2002). Though fjords and glaciers act as partial barriers to gene flow among the native and introduced subspecies, Jepsen et al. (2002) found evidence for introgression. Microsatellite markers characteristic for R. t. groenlandicus and R. t. tarandus were found to have introgressed between the geographically overlapping caribou and reindeer populations (Jepsen et al. 2002). The finding of significant introgression between native caribou and introduced reindeer in Greenland contrasts with findings for native and introduced forms in Alaska. In the latter study, Cronin et al. (2003) concluded that ‘… there may have been a low level of introgression, but the two forms have maintained different allele frequencies over the 110 years since the introduction of reindeer to Alaska.’ Yet these authors did report a high level of genetic similarity between arctic Canadian caribou from Baffin Island and Scandinavian reindeer populations (Cronin et al. 2003). I hypothesize that such a relationship would be expected if gene flow had occurred between the caribou population on Baffin Island and semidomesticated reindeer.

The wild and domesticated water buffalo assemblage also illustrates the role of hybridization between ancestral and derivative taxa. As discussed previously, the domestication of individual plant and animal taxa often occurs in multiple geographical regions. This results in polyphyletic domesticated taxa, i.e. domesticated forms founded from multiple, independent wild lineages. Such is the case for pigs, cattle and sheep (see above discussion). This historical pattern is also apparent for domesticated water buffalo in which there are two morphologically, and genetically, recognizable types — the river and swamp forms (Sena et al. 2003). Lau et al. (1998) postulated that the swamp variant represented the ancestral water buffalo phenotype. Furthermore, they posited that this form arose in Asia and spread to the Indian subcontinent where the river buffalo evolved. Following the divergence of the river and swamp forms, two domesticated stocks arose from the two centres of water buffalo evolution. The domesticated, swamp buffalo then extended its range through mainland Southeast Asia with the concomitant result of ‘… interbreeding with wild buffalo …’ populations (Lau et al. 1998).

Introgressive hybridization can result in a higher degree of similarity between progenitor and derivative (i.e. domesticated) forms than predicted by a simple, divergent model of evolution. Introgression may thus cause the convergence of the evolutionary trajectories of the wild and domesticated taxa. In addition, natural hybridization between progenitor and domesticated taxa may result in the genetic enrichment of the domesticated populations. This may be of even greater significance due to the extreme population bottlenecks, and accompanying reduction in genetic variability, through which domesticated forms are likely to pass. The reindeer and water buffalo taxa may reflect such genetic enrichment. However, in animal systems, possibly the best illustration comes from studies of wild and domestic canids (Vilàet al. 1997, 1999; Irion et al. 2003).

Two hypotheses have been proposed to explain the extreme morphological variation present in domestic dogs: (i) dogs originated from a limited number of wild progenitors and the phenotypic variation present in different breeds reflects mutations that arose after their derivation from wild populations; or (ii) dogs originated from a large number of wild progenitors, have hybridized periodically with these ancestors since their domestication, and the variation found in contemporary breeds is due largely to introgression from wild populations (Vilàet al. 1999).

Results from genetic analyses of domestic and wild canids allow several conclusions. First, domestic dog breeds demonstrate extremely high levels of mitochondrial (Vilàet al. 1997, 1999; Leonard et al. 2002; Savolainen et al. 2002) and nuclear (Kim et al. 2001; Irion et al. 2003) DNA variation. Second, the domestication of dogs may have occurred as much as 100 000 years bp, rather than the 14 000 years suggested by archeological remains (Vilàet al. 1997; Leonard et al. 2002; but see Savolainen et al. 2002). Third, the immediate ancestor of domestic dogs is the grey wolf (Vilàet al. 1997; Leonard et al. 2002). Fourth, derivation of domestic dog lineages occurred multiple times from grey wolf populations (Vilàet al. 1997, 1999; Savolainen et al. 2002). Fifth, subsequent to their origin, domestic dogs have been introgressed by wolf genomic elements (Fig. 3). These observations led Vilàet al. (1997) to conclude the following: ‘Repeated genetic exchange between dog and wolf populations may have been an important source of variation for artificial selection’. The findings from each of the genetic analyses of domestic dogs and their wild progenitors thus support the second of the two hypotheses listed above; domestic dogs have been periodically enriched via introgression from wild populations.

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Figure 3. A neighbour-joining tree illustrating relationships between wolf (W) and domestic dog (D) mitochondrial control region haplotypes. Only bootstrap values exceeding 50% are shown (from Vilàet al. 1997).

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Natural hybridization and the evolution of pathogens, pests and vectors

  1. Top of page
  2. Abstract
  3. Introduction
  4. Introgressive hybridization and the evolution of domesticated plants
  5. Introgressive hybridization and the development of domesticated animals
  6. Natural hybridization and the evolution of pathogens, pests and vectors
  7. Concluding remarks
  8. Acknowledgements
  9. References

As stated previously, natural hybridization has played an important role in the evolutionary history of numerous taxa of plants and animals (e.g. Arnold 1992, 1997; Grant & Grant 1992; Dowling & DeMarais 1993; Rieseberg 1997). However, I am unaware of a review that has focused on how this process has affected the origin and evolution of organisms that negatively impact human populations. In the following sections I discuss several examples for which natural hybridization has been shown to be so involved. In particular, I address the following questions:

  • 1
    Has natural hybridization led to the origin of pathogens and pests that attack agricultural or natural plant populations that are important to humans?
  • 2
    Is it probable that introgressive hybridization is a factor in the expansion of the geographical/ecological range of pests, pathogens and disease vectors?

In the course of this discussion, I emphasize those instances where this process leads to the same type of evolutionary creativity detected for nonpest/nonpathogenic complexes.

The origin of plant pathogens and pests through natural hybridization

Brasier et al. (1999) observed that ‘Plant disease epidemics resulting from introductions of exotic fungal pathogens are a well known phenomenon.’ However, they also concluded that ‘An associated risk — that accelerated pathogen evolution may be occurring as a consequence of genetic exchange between introduced, or introduced and resident, fungal pathogens — is largely unrecognized.’ Though this quote is concerned with one of our current topics, i.e. plant pathogen evolution, it summarizes well the conclusion provided at the outset of this review, that certain roles played by natural hybridization in the evolution of species complexes remain under appreciated (Arnold et al. 1999; Burke & Arnold 2001; Arnold & Burke 2004). Brasier et al. (1999) reflected on the importance of testing for the action of natural hybridization in the evolution of plant pathogens because the outcome of such crosses can include ‘… the acquisition of new host specificities …’ and the ‘… emergence of entirely new pathogen taxa.’ Both types of outcomes have been postulated for nonpathogenic species. The evolution of ecological diversity and the origin of new species via hybridization and introgression have thus been detected in numerous species complexes (e.g. Arnold 1997; Rieseberg 1997; Schweitzer et al. 2002; Rieseberg et al. 2003).

The origin of virulent, fungal species is of the utmost concern for both cultivated and natural ecosystems. The formation of plant, fungal pathogens through natural hybridization is exemplified well by its occurrence in Phytophthora. This fungal genus includes species that attack cultivars (e.g. potato blight) and native species (e.g. forest dieback; Brasier et al. 1999). Significantly, pathogenic variants from the Phytophthora complex were found to be (i) hybrid derivatives and (ii) genetically very similar to the nonpathogenic species, Phytophthora cambivora (Brasier et al. 1999). However, three years after their discovery the hybrids were already responsible for the deaths of more than 10 000 trees (Brasier et al. 1999). Though the tree species affected (i.e. riparian alders) were not a human food source, they were a significant member of an important ecosystem and as such were critical for conservation efforts. This example illustrates a negative effect of plant pathogens on human populations, other than in attacking food sources.

The origin of the pathogenic Phytophthora via natural hybridization between nonpathogens is of particular importance in understanding evolutionary processes and disease control. On the one hand, this occurrence demonstrates the potential for natural hybridization to produce new fungal lineages that possess novel phenotypes and ecological amplitudes (e.g. Tsai et al. 1994; O’Donnell & Cigelnik 1997; Brasier et al. 1999). On the other hand, though the origin of some fungal lineages via hybridization may lead to beneficial interactions (e.g. plant endosymbionts; Tsai et al. 1994), the origin of pathogens obviously poses a threat to artificial and natural ecosystems (Brasier et al. 1999). Both the positive and negative outcomes (for human populations) reflect a recurring hypothesis in the natural hybridization literature; introgression may produce hybrid genotypes possessing novel ecological adaptations allowing their occupation of niches different from their progenitors (Anderson 1948, 1949; Anderson & Stebbins 1954).

Like plant pathogens, some plant pests also show the effect of natural hybridization and introgression. For example, Lewontin & Birch (1966) concluded that the evolution of the Australian fruit fly pests, Bactrocera tryoni and B. neohumeralis (formerly Dacus tryoni and D. neohumeralis) included reticulation. These authors proposed that introgression from B. neohumeralis into B. tryoni allowed the latter species to expand its range and impact additional areas of cultivated fruit species. According to Lewontin & Birch (1966) the footprints of this process included (i) the introgression of a morphological marker and (ii) outbreaks of B. tryoni on both temperate crops such as apples, peaches and various citrus taxa as well as tropical fruit species such as guavas. It was subsequently argued that this hypothesis was likely incorrect (Gibbs 1968; Birch & Vogt 1970). However, recent applications of molecular genetic markers have supported the original conclusion that B. neohumeralis genes have introgressed into B. tryoni (Morrow et al. 2000). Indeed, Pike et al. (2003) demonstrated that introgression between these two species is likely to be asymmetric, from B. neohumeralis into B. tryoni, because there is a difference in mating time for the two species and the F1 and backcross 1 hybrids mate when B. tryoni is active (Pike et al. 2003). Thus, the hypothesis that introgression can expand greatly a pest species’ niche (Lewontin & Birch 1966) is supported by findings from the Bactrocera complex.

Introgressive hybridization and the evolution of the human disease vector Anopheles gambiae

Though each of the above sections illustrates the widespread impact of natural hybridization, the effect of this process on the evolution of organisms that impact human populations may be most readily apparent when we consider vectors of human diseases and human diseases themselves. The role of this process in the evolution of such organisms is obvious due to the ensuing human suffering. However, I argue that the unique outcome of this process for vectors and pathogens, as measured in disease and death tolls, does not reflect different evolutionary mechanisms. The generation of novel genotypes and phenotypes is the basis of geographical spread, ecological shifts and the origin of new taxa of disease vectors and diseases, just as it is the starting point for the same evolutionary and ecological outcomes in other natural and domesticated populations.

The Anopheles gambiae species complex includes the major malarial vectors, An. gambiae and An. arabiensis. It also encompasses taxa, such as An. melas, An. merus, An. bwambae and An. quadriannulatus, which are not considered to be major routes for malaria transmission (Besansky et al. 2003). Significant genetic discontinuities, indicating a level of subspecific reproductive isolation, have been detected within the widespread An. gambiae (Gentile et al. 2002). Further support for the presence of reproductive barriers within this species comes from the co-occurrence of different genotypes at the rDNA cistron. The variation in rDNA nucleotide sequence was discovered within both the internal transcribed spacer (ITS) and intergenic spacer (IGS) regions (Gentile et al. 2002). The detection of (i) no heterozygotes for the different variants and (ii) nearly total linkage disequilibrium for the pairs of ITS and IGS genotypes defined as ‘S/type I’ and ‘M/type II’ indicated that these races were partially, reproductively isolated (Gentile et al. 2002). In contrast, other regions of the genome demonstrated no such genetic discontinuities (Wang et al. 2001; Gentile et al. 2002). These contrasting patterns indicate that the S and M genomes are ‘semipermeable’ (Key 1968), with some regions recombining at a high frequency and others, like the rDNA cistron, recombining rarely.

The concept of semipermeability can also be applied across the An. gambiae species complex. For example, two earlier studies of the genetic architecture of the sibling species, An. gambiae and An. arabiensis, reported limited (Lanzaro et al. 1998) and extensive (Besansky et al. 1997) introgression of nuclear and mitochondrial genetic markers, respectively (Fig. 4). More recent studies have confirmed the observation of ongoing genetic exchange between these two species (Wang et al. 2001; Besansky et al. 2003). With regard to the current topic, the most important hypothesis was stated in the following manner by Besansky et al. (2003): ‘The proposed acquisition by An. gambiae of sequences from the more arid-adapted An. arabiensis may have contributed to the spread and ecological dominance of this malaria vector.’ Like, for example, landraces of maize and Australian fruit flies, the increase in ecological amplitude and the subsequent spread of a major disease vector may have been caused by introgressive hybridization.

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Figure 4. Relationships among 59 mtDNA haplotypes identified from the ND5 genes of Anopheles gambiae and An. arabiensis. The white and black circles indicate haplotypes that are found only in An. gambiae or An. arabiensis, respectively. Hatched circles indicate haplotypes that are found in both species. The size of each circle is proportional to its frequency, and the connections between circles reflect one nucleotide difference. A ‘0’ along a branch indicates a missing variant (from Besansky et al. 1997).

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Natural hybridization and the origin of human pathogens

Not only do disease vectors such as An. gambiae demonstrate the potential evolutionary and epidemiological effects of natural hybridization, but so do human diseases. Recombination between divergent microorganisms, microorganisms that may not themselves cause serious diseases, giving rise to novel human pathogens has been proposed for protozoan, fungal, viral and bacterial systems (e.g. Kroll et al. 1998; Cogliati et al. 2001; Gibbs et al. 2001; Machado & Ayala 2001; Webster 2001; Smoot et al. 2002; Laird et al. 2003).

Trypanosoma cruzi is the protozoan parasite that causes Chagas’ disease, otherwise known as American trypanosomiasis. The Centers for Disease Control and Prevention (CDC website 2003) estimate that 16–18 million people are infected with T. cruzi and that each year 50 000 will die from the infection. It has long been recognized that this protozoan species is both genetically and phenotypically highly variable (Machado & Ayala 2001). Using an analysis of sequence variation at unlinked genes, Machado & Ayala (2001) were able to test whether this variability was due to natural hybridization. They concluded that natural hybridization had affected this species complex. Indeed, the important evolutionary role played by natural hybridization in the T. cruzi lineage is summarized by the following quote: ‘The results provide evidence of hybridization between strains from two divergent groups of T. cruzi, demonstrate mitochondrial introgression across distantly related lineages, and reveal genetic exchange among closely related strains’ (Machado & Ayala 2001). The basis of the genetic and phenotypic (e.g. growth rate, pathogenicity, infectivity, drug susceptibility) variability within T. cruzi appears to be recombination following hybridization between divergent lineages.

Cryptococcus neoformans is a human fungal pathogen that causes meningitis in both immunocompetent and immunocompromised individuals (Cogliati et al. 2001). Between 0.2 and 0.9 infections per 100 000 persons occur in the general population and between 2 and 4 infections per 1000 occur among persons with AIDS. The overall mortality rate is ~12% (CDC website 2003). As with T. cruzi, C. neoformans demonstrates a high level of genetic variability (Cogliati et al. 2001). Though normally haploid, diploid isolates have been identified from the recognized varieties of C. neoformans (Cogliati et al. 2001). The origin of these diploid recombinants from crosses between the various haploid serotypes was thought to be rare. However, an analysis of sequence variation (Cogliati et al. 2001) demonstrated that these derivatives of hybridization were actually quite common. Forty-nine diploid strains were identified from a sample of 133 isolates gathered from Italian patients. These findings indicated that, like T. cruzi, evolution of the C. neoformans complex had been impacted greatly by the transfer of genetic material via natural hybridization. Such is also the case for the evolution of viral pathogens.

Viral lineages play an enormous role in human diseases. For example, viruses have caused some of the most catastrophic pandemics. Many diseases that emaciate, and thus make humans susceptible to death by secondary causes, are also of viral origin. The human rotavirus is an example of this latter class of pathogen. Human rotaviruses have the distinction of being the most common cause of severe diarrhoea in infants and young children, causing an estimated 600 000 deaths per year (Laird et al. 2003; CDC website 2003). These viruses are widely distributed among animal species, however, prior to a DNA sequence analysis by Laird et al. (2003) the strains were thought to be restricted to a single species, with no transmission from other animal species to humans. In contrast to this paradigm, Laird et al. (2003) detected not one, but two apparent recombination events. These cases of hybridization resulted in the origin of two diverse rotavirus lineages found in infected humans. The two strains have combinations of human and canine and human and porcine DNA segments, respectively (Laird et al. 2003). It is apparent that not only is transmission possible between the different animal species, but variants of this highly pathogenic viral assemblage have arisen through subsequent recombination.

The 1918 ‘Spanish flu’ is one of the best known, and most lethal, human viral pandemics. Significantly, Gibbs et al. (2001) have proposed a hybrid origin for the influenza variant that caused this major outbreak. Like some of the rotavirus strains, the ‘Spanish flu’ virus was hypothesized to have arisen from hybridization between human and swine viral genomes. In contrast, Basler et al. (2001) proposed that the virus causing the 1918 pandemic was not of hybrid origin, but was instead introduced from an avian source into both swine and humans shortly before 1918. The uncertainty concerning the hybrid origin of the 1918 influenza outbreak does not extend to those epidemics occurring in 1957 and 1968. These two pandemics also killed millions, but were definitively found to be of hybrid origin. In both cases, recombination between avian and human influenza strains gave rise to these lethal pathogens (see Webster 2001 for a discussion). These findings suggest that the 1957 and 1968 outbreaks were due to hybridization that brought together genes from divergent lineages thus causing their increased pathogenicity to humans.

Our final example of human pathogens formed from hybridization and recombination comes from the bacterial complex, Haemophilus influenzae. This bacterial species is one of the most common microorganisms in the upper respiratory tract of humans (Kroll et al. 1998). It is also normally benign, but sometimes invades leading to serious illnesses most often in children. One of the diseases for which this species has been implicated is Brazilian purpuric fever. The name of this disease reflects its original detection within a Brazilian population of infected children, 70% of who died from its effects. However, the description of the clinical features of this novel disease, i.e. meningococcal sepsis, suggested initially the involvement of a meningococcus species (Kroll et al. 1998). Surprisingly, the disease was found instead to be the result of infection by H. influenzae biogroup aegyptius, an organism that had previously been known to cause nothing more serious than conjunctivitis (Kroll et al. 1998). This novel H. influenzae had thus somehow acquired the meningococcal phenotype. Kroll et al. (1998) hypothesized that the evolution of this novel phenotype was due to the transfer of virulence genes from Neisseria meningitidis into H. influenzae (Fig. 5). Smoot et al. (2002) subsequently found evidence for such hybridization and recombination between these different genera. The increase in pathogenicity of H. influenzae is conceptually similar to the increase in ecological amplitude of, for example, maize landraces; both increases are thought to reflect the acquisition of traits from related organisms allowing the invasion of additional adaptive space. However, unlike the positive benefits derived from the maize introgression events, the derivation of pathogenic H. influenzae biogroup aegyptius illustrate the origin through hybridization of a ‘… clone with the phenotype of rapidly fatal invasive infection …’ (Kroll et al. 1998).

image

Figure 5. Gene trees derived from (A) the protein and (B) 16S RNA sequences of the bacterial species Haemophilus influenzae (H), Neisseria meningitidis (N) and Escherichia coli (E). Numbers along the branches indicate the number of mutational steps between the terminal taxa (from Kroll et al. 1998).

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Concluding remarks

  1. Top of page
  2. Abstract
  3. Introduction
  4. Introgressive hybridization and the evolution of domesticated plants
  5. Introgressive hybridization and the development of domesticated animals
  6. Natural hybridization and the evolution of pathogens, pests and vectors
  7. Concluding remarks
  8. Acknowledgements
  9. References

I believe that this review has demonstrated the involvement of natural hybridization, in its broadest sense, in the formation of some of humankind's best assets and worst banes. However, though the examples given in this review strongly implicate the role of natural hybridization in the formation of numerous taxa that positively and negatively impact humankind, only a subset of studies reflect strong inferences concerning when and how this impact has come about. For example, it is clear that introgressive hybridization between wolf and domesticated dogs is an ongoing process. Yet, whether or not this introgression is indicative of ancient, or more recent, contact remains a mystery. Likewise, the high genetic similarity between various livestock species and their wild progenitors (e.g. wild mouflon and domesticate sheep) may be the result of the retention of feral populations mistaken for wild species or ongoing introgression between domesticated and wild populations. Such conundrums should, however, be solvable through the analysis of additional loci and populations.

The question of causality also presents investigators with a myriad of difficult hypotheses. Thus, maize landraces occurring at higher than normal elevations and An. gambiae populations spreading into arid habitats may be due to introgression from high elevation-adapted and arid-adapted taxa, respectively. Alternatively, the detected introgression and the spread of taxa into novel habitats may be merely coincidental. Similarly, the invasiveness of hybrid pathogens may be due to their hybridity, or to mutations at single genes inherited from only one of the parental taxa. Determining whether or not natural hybridization has been causal in these and other examples will require experimentation to define the effects of introduced genes, whether in crop plants, livestock, plant pests, disease vectors or human pathogens.

Acknowledgements

  1. Top of page
  2. Abstract
  3. Introduction
  4. Introgressive hybridization and the evolution of domesticated plants
  5. Introgressive hybridization and the development of domesticated animals
  6. Natural hybridization and the evolution of pathogens, pests and vectors
  7. Concluding remarks
  8. Acknowledgements
  9. References

The author wishes to thank A. Bouck and S. Cornman for comments on an earlier draft. The author is also grateful to L. Rieseberg for bringing the pandemic virus examples to his attention. During the preparation of this review, the author was supported by NSF grant DEB-0074159.

References

  1. Top of page
  2. Abstract
  3. Introduction
  4. Introgressive hybridization and the evolution of domesticated plants
  5. Introgressive hybridization and the development of domesticated animals
  6. Natural hybridization and the evolution of pathogens, pests and vectors
  7. Concluding remarks
  8. Acknowledgements
  9. References
  • Anderson E (1948) Hybridization of the habitat. Evolution, 2, 19.
  • Anderson E (1949) Introgressive Hybridization. Wiley, New York.
  • Anderson E, Stebbins GL Jr (1954) Hybridization as an evolutionary stimulus. Evolution, 8, 378388.
  • Arnold ML (1992) Natural hybridization as an evolutionary process. Annual Review of Ecology and Systematics, 23, 237261.
  • Arnold ML (1997) Natural Hybridization and Evolution. Oxford University Press, Oxford.
  • Arnold ML, Bulger MR, Burke JM, Hempel AL, Williams JH (1999) Natural hybridization — how low can you go? (and still be important). Ecology, 80, 371381.
  • Arnold ML, Burke JM (2004) Natural hybridization. In: Evolutionary Genetics: Concepts and Case Studies (eds FoxCW, WolfJB). Oxford University Press, Oxford, in press.
  • Basler CF, Reid AH, Dybing JK et al. (2001) Sequence of the 1918 pandemic influenza virus nonstructural gene (NS) segment and characterization of recombinant viruses bearing the 1918 NS genes. Proceedings of the National Academy of Sciences of the USA, 98, 27462751.
  • Besansky NJ, Krzywinski J, Lehmann T et al. (2003) Semipermeable species boundaries between Anopheles gambiae and Anopheles arabiensis: evidence from multilocus DNA sequence variation. Proceedings of the National Academy of Sciences of the USA, 100, 1081810823.
  • Besansky NJ, Lehmann T, Fahey GT et al. (1997) Patterns of mitochondrial variation within and between African malaria vectors, Anopheles gambiae and An. arabiensis, suggest extensive gene flow. Genetics, 147, 18171828.
  • Birch LC, Vogt WG (1970) Plasticity of taxonomic characters of the Queensland fruit flies Dacus tryoni and Dacus neohumeralis (Tephritidae). Evolution, 24, 320343.
  • Brasier CM, Cooke DEL, Duncan JM (1999) Origin of a new Phytophthora pathogen through interspecific hybridization. Proceedings of the National Academy of Sciences of the USA, 96, 58785883.
  • Burke JM, Arnold ML (2001) Genetics and the fitness of hybrids. Annual Review of Genetics, 35, 3152.
  • Burke JM, Rieseberg LH (2003) Fitness effects of transgenic disease resistance in sunflowers. Science, 300, 1250.
  • Cogliati M, Esposoto MC, Clarke DL, Wickes BL, Viviani MA (2001) Origin of Cryptococcus neoformans var. neoformans diploid strains. Journal of Clinical Microbiology, 39, 38893894.
  • Coulibaly S, Pasquet RS, Papa R, Gepts P (2002) AFLP analysis of the phenetic organization and genetic diversity of Vigna unguiculata L. Walp. Reveals extensive gene flow between wild and domesticated types. Theoretical and Applied Genetics, 104, 358366.
  • Cronin MA, Patton JC, Balmysheva N, MacNeil MD (2003) Genetic variation in caribou and reindeer (Rangifer tarandus). Animal Genetics, 34, 3341.
  • Desplanque B, Boudry P, Broomberg K, Saumitou-Laprade P, Cuguen J, Van Dijk H (1999) Genetic diversity and gene flow between wild, cultivated and weedy forms of Beta vulgaris L. (Chenopodiaceae), assessed by RFLP and microsatellite markers. Theoretical and Applied Genetics, 98, 11941201.
  • Doebley J, Stec A, Gustus C (1995) Teosinte branched1 and the origin of maize: evidence for epistasis and the evolution of dominance. Genetics, 141, 333346.
  • Doebley J, Stec A, Hubbard L (1997) The evolution of apical dominance in maize. Nature, 386, 485488.
  • Dowling TE, DeMarais BD (1993) Evolutionary significance of introgressive hybridization in cyprinid fishes. Nature, 362, 444446.
  • Ellstrand NC (2003) Dangerous Liaisons? When Cultivated Plants Mate with Their Wild Relatives. Johns Hopkins University Press, Baltimore.
  • Ellstrand NC, Prentice HC, Hancock JF (1999) Gene flow and introgression from domesticated plants into their wild relatives. Annual Review of Ecology and Systematics, 30, 539563.
  • Ellstrand NC, Schierenbeck KA (2000) Hybridization as a stimulus for the evolution of invasiveness in plants. Proceedings of the National Academy of Sciences of the USA, 97, 70437050.
  • Gentile G, Della Torre A, Maegga B, Powell JR, Caccone A (2002) Genetic differentiation in the African malaria vector, Anopheles gambiae s.s. and the problem of taxonomic status. Genetics, 161, 15611578.
  • Gibbs GW (1968) The frequency of interbreeding between two sibling species of Dacus (Diptera) in wild populations. Evolution, 22, 667683.
  • Gibbs MJ, Armstrong JS, Gibbs AJ (2001) Recombination in the hemagglutinin gene of the 1918 ‘Spanish Flu’. Science, 293, 18421845.
  • Giuffra E, Kijas JMH, Amarger V, Carlborg Ö, Jeon J-T, Andersson L (2000) The origin of the domestic pig: independent domestication and subsequent introgression. Genetics, 154, 17851791.
  • Grant PR, Grant BR (1992) Hybridization of bird species. Science, 256, 193197.
  • Grant PR, Grant BR (2002) Unpredictable evolution in a 30-year study of Darwin's finches. Science, 296, 707711.
  • Grant V (1981) Plant Speciation. Columbia University Press, New York.
  • Harrison RG (1990) Hybrid zones: windows on evolutionary process. Oxford Surveys in Evolutionary Biology, 7, 69128.
  • Hiendleder S, Kaupe B, Wassmuth R, Janke A (2002) Molecular analysis of wild and domestic sheep questions current nomenclature and provides evidence for domestication from two different subspecies. Proceedings of the Royal Society of London, B, 269, 893904.
  • Hiendleder S, Mainz K, Plante Y, Lewalski H (1998) Analysis of mitochondrial DNA indicates that domestic sheep are derived from two different ancestral maternal sources: no evidence for contributions from urial and argali sheep. Journal of Heredity, 89, 113120.
  • Howard DJ (1993) Reinforcement: origin, dynamics, and fate of an evolutionary hypothesis. In: Hybrid Zones and the Evolutionary Process (ed. HarrisonRG), pp. 4669. Oxford University Press, Oxford.
  • Huang S, Sirikhachornkit A, Su X et al. (2002) Genes encoding plastid acetyl-CoA carboxylase and 3-phosphoglycerate kinase of the Triticum/Aegilops complex and the evolutionary history of polyploid wheat. Proceedings of the National Academy of Sciences of the USA, 99, 81338138.
  • Husband BC, Schemske DW (1998) Cytotype distribution at a diploid–tetraploid contact zone in Chamerion (Epilobium) angustifolium (Onagraceae). American Journal of Botany, 85, 16881694.
  • Irion DN, Schaffer AL, Famula TR, Eggleston ML, Hughes SS, Pedersen NC (2003) Analysis of genetic variation in 28 dog breed populations with 100 microsatellite markers. Journal of Heredity, 94, 8187.
  • Jepsen BI, Siegismund HR, Fredholm M (2002) Population genetics of the native caribou (Rangifer tarandus groenlandicus) and the semi-domestic reindeer (Rangifer tarandus tarandus) in southwestern Greenland: evidence of introgression. Conservation Genetics, 3, 401409.
  • Johnston JA, Arnold ML, Donovan LA (2003) High hybrid fitness at seed and seedling life history stages in Louisiana Irises. Journal of Ecology, 91, 438446.
  • Kadwell M, Fernandez M, Stanley HF et al. (2001) Genetic analysis reveals the wild ancestors of the llama and the alpaca. Proceedings of the Royal Society of London, B, 268, 25752584.
  • Key KHL (1968) The concept of stasipatric speciation. Systematic Zoology, 17, 1422.
  • Kijas JMH, Andersson L (2001) A phylogenetic study of the origin of the domestic pig estimated from the near-complete mtDNA genome. Journal of Molecular Evolution, 52, 302308.
  • Kim KS, Tanabe Y, Park CK, Ha JH (2001) Genetic variability in East Asian dogs using microsatellite loci analysis. Journal of Heredity, 92, 398403.
  • Kim K-I, Yang Y-H, Lee S-S et al. (1999) Phylogenetic relationships of Cheju horses to other horse breeds as determined by mtDNA d-loop sequence polymorphism. Animal Genetics, 30, 102108.
  • Kroll JS, Wilks KE, Farrant JL, Langford PR (1998) Natural genetic exchange between Haemophilus and Neisseria: intergenic transfer of chromosomal genes between major human pathogens. Proceedings of the National Academy of Sciences of the USA, 95, 1238112385.
  • Laird AR, Ibarra V, Ruiz-Palacios G, Guerrero ML, Glass RI, Gentsch JR (2003) Unexpected detection of animal VP7 genes among common Rotavirus strains isolated from children in Mexico. Journal of Clinical Microbiology, 41, 44004403.
  • Lanzaro GC, Touré YT, Carnahan J et al. (1998) Complexities in the genetic structure of Anopheles gambiae populations in west Africa as revealed by microsatellite DNA analysis. Proceedings of the National Academy of Sciences of the USA, 95, 1426014265.
  • Lau CH, Drinkwater RD, Yusoff K, Tan SG, Hetzel DJS, Barker JSF (1998) Genetic diversity of Asian water buffalo (Bubalus bubalus): mitochondrial DNA d-loop and cytochrome b sequence variation. Animal Genetics, 29, 253264.
  • Leonard JA, Wayne RK, Wheeler J, Valadez R, Guillén S, Vilà C (2002) Ancient DNA evidence for Old World origin of New World dogs. Science, 298, 16131616.
  • Lewis CS (1954) English Literature in the Sixteenth Century. Oxford University Press, Oxford.
  • Lewontin RC, Birch LC (1966) Hybridization as a source of variation for adaptation to new environments. Evolution, 20, 315336.
  • Luikart G, Gielly L, Excoffier L, Vigne J-D, Bouvet J, Taberlet P (2001) Multiple maternal origins and weak phylogeographic structure in domestic goats. Proceedings of the National Academy of Sciences of the USA, 98, 59275932.
  • Machado CA, Ayala FJ (2001) Nucleotide sequences provide evidence of genetic exchange among distantly related lineages of Trypanosoma cruzi. Proceedings of the National Academy of Sciences of the USA, 98, 73967401.
  • MacHugh DE, Bradley DG (2001) Livestock genetic origins: goats buck the trend. Proceedings of the National Academy of Sciences of the USA, 98, 53825384.
  • MacHugh DE, Shriver MD, Loftus RT, Cunningham P, Bradley DG (1997) Microsatellite DNA variation and the evolution, domestication and phylogeography of Taurine and Zebu cattle (Bos taurus and Bos indicus). Genetics, 146, 10711086.
  • Matsuoka Y, Vigouroux Y, Goodman MMG, Sanchez J, Buckler E, Doebley J (2002) A single domestication for maize shown by multilocus microsatellite genotyping. Proceedings of the National Academy of Sciences of the USA, 99, 60806084.
  • Morrow J, Scott L, Congdon B, Yeates D, Frommer M, Sved J (2000) Close genetic similarity between two sympatric species of Tephritid fruit fly reproductively isolated by mating time. Evolution, 54, 899910.
  • O'Donnell K, Cigelnik E (1997) Two divergent intragenomic rDNA ITS2 types within a monophyletic lineage of the fungus Fusarium are nonorthologous. Molecular Phylogenetics and Evolution, 7, 103116.
  • Papa R, Gepts P (2003) Asymmetry of gene flow and differential geographical structure of molecular diversity in wild and domesticated common bean (Phaseolus vulgaris L.) from Mesoamerica. Theoretical and Applied Genetics, 106, 239250.
  • Paszek AA, Flickinger GH, Fontanesi L et al. (1998) Evaluating evolutionary divergence with microsatellites. Journal of Molecular Evolution, 46, 121126.
  • Pike N, Wang W, Meats A (2003) The likely fate of hybrids of Bactrocera tryoni and Bactrocera neohumeralis. Heredity, 90, 365370.
  • Rieseberg LH (1997) Hybrid origins of plant species. Annual Review of Ecology and Systematics, 28, 359389.
  • Rieseberg LH, Raymond O, Rosenthal DM et al. (2003) Major ecological transitions in wild sunflowers facilitated by hybridization. Science, 301, 12111216.
  • Santalla M, Rodiño AP, De Ron AM (2002) Allozyme evidence supporting southwestern Europe as a secondary center of genetic diversity for the common bean. Theoretical and Applied Genetics, 104, 934944.
  • Savolainen P, Zhang Y, Luo J, Lundeberg J, Leitner T (2002) Genetic evidence for an East Asian origin of domestic dogs. Science, 298, 16101613.
  • Schemske DW (2000) Understanding the origin of species. Evolution, 54, 10691073.
  • Schweitzer JA, Martinsen GD, Whitham TG (2002) Cottonwood hybrids gain fitness traits of both parents: a mechanism for their long-term persistence? American Journal of Botany, 89, 981990.
  • Sena L, Schneider MPC, Brenig B, Honeycutt RL, Womack JE, Skow LC (2003) Polymorphisms in MHC-DRA and -DRB alleles of water buffalo (Bubalus bubalus) reveal different features from cattle DR alleles. Animal Genetics, 34, 110.
  • Smoot LM, Franke DD, McGillivary G, Actis LA (2002) Genomic analysis of the F3031 Brazilian purpuric fever clone of Haemophilus influenzae biogroup Aegyptius by PCR-based subtractive hybridization. Infection and Immunity, 70, 26942699.
  • Talbert LE, Doebley JF, Larson S, Chandler VL (1990) Tripsacum andersonii is a natural hybrid involving Zea and Tripsacum: molecular evidence. American Journal of Botany, 77, 722726.
  • Toumi L, Lumaret R (1998) Allozyme variation in cork oak (Quercus suber L.): the role of phylogeography and genetic introgression by other Mediterranean oak species and human activities. Theoretical and Applied Genetics, 97, 647656.
  • Tsai H-F, Liu J-S, Staben C et al. (1994) Evolutionary diversification of fungal endophytes of tall fescue grass by hybridization with Epichloë species. Proceedings of the National Academy of Sciences of the USA, 91, 25422546.
  • Viard F, Bernard J, Desplanque B (2002) Crop–weed interactions in the Beta vulgaris complex at a local scale: allelic diversity and gene flow within sugar beet fields. Theoretical and Applied Genetics, 104, 688697.
  • Vilà C, Leonard JA, Götherström A et al. (2001) Widespread origins of domestic horse lineages. Science, 291, 474477.
  • Vilà C, Maldonado JE, Wayne RK (1999) Phylogenetic relationships, evolution, and genetic diversity of the domestic dog. Journal of Heredity, 90, 7177.
  • Vilà C, Savolainen P, Maldonado JE et al. (1997) Multiple and ancient origins of the domestic dog. Science, 276, 16871689.
  • Wang R, Zheng L, Touré YT, Dandekar T, Kafatos FC (2001) When genetic distance matters: measuring genetic differentiation at microsatellite loci in whole-genome scans of recent and incipient mosquito species. Proceedings of the National Academy of Sciences of the USA, 98, 1076910774.
  • Webster RG (2001) A molecular whodunit. Science, 293, 17731775.
  • Xu DH, Abe J, Gai JY, Shimamoto Y (2002) Diversity of chloroplast DNA SSRs in wild and cultivated soybeans: evidence for multiple origins of cultivated soybean. Theoretical and Applied Genetics, 105, 645653.