Adaptation by introgression
© BioMed Central Ltd 2009
Published: 13 October 2009
Both selective and random processes can affect the outcome of natural hybridization. A recent analysis in BMC Evolutionary Biology of natural hybridization between an introduced and a native salamander reveals the mosaic nature of introgression, which is probably caused by a combination of selection and demography.
Natural interspecific hybridization has been observed in a diverse array of taxa [1–3], and the production of such hybrids can have a wide range of evolutionary consequences. For instance, natural hybridization can act as a 'destructive' force, resulting in the fusion of taxa that do not reveal strong reproductive isolation . Alternatively, it can result in evolutionary novelty via the production of new reproductively isolated hybrid species [1–3], or by the transfer of potentially adaptive traits through a process known as introgressive hybridization. In a recent article in BMC Evolutionary Biology, Fitzpatrick et al.  tested for introgressive hybridization by performing a genome-wide scan of native salamander (Ambystoma californiense) populations, and identified genomic regions that have rapidly fixed alternative alleles derived from a recently introduced, invasive species (Ambystoma mavortium). This rapid assimilation of non-native alleles suggests that selective processes were involved in their fixation.
Introgressive hybridization is a multi-step process by which genetic material from one population infiltrates into another, genetically differentiated population . In order for introgressive hybridization to take place, F1 hybrids must initially be produced between the two species. In nature, such hybrid formation is often a rare event owing to the presence of multiple prezygotic and postzygotic reproductive barriers , and indeed in most species-pairs studied to date, the frequencies of F1 hybrid formation are low . However, even if the F1 hybrids possess only partial fitness, they may mate with one or both progenitor species to produce first-generation backcross (BC1) hybrids. These BC1 hybrids may further backcross with pure-species individuals, ultimately resulting in the transfer of novel alleles between the hybridizing lineages/species .
A key question with respect to introgressive hybridization is 'To what degree is interspecific gene flow the result of adaptive processes?' Whereas hybridization can certainly result in the transfer of alleles and traits across species boundaries , such genetic exchange does not necessarily involve the transfer of adaptations. Stochastic processes (that is, random genetic drift) could potentially explain introgression events, and deciphering the roles of stochastic and deterministic (that is, natural selection) processes has often proved difficult. Only a handful of examples are currently available that provide rigorous tests for adaptive introgression [6–11]. Given the scarcity of such analyses, the recent study of Fitzpatrick et al.  reporting on signatures of adaptive introgression in salamanders is a significant contribution. Here, we review four examples (including ) that have used four different methodologies to test for adaptive introgression.
Evidence for adaptive introgression in plants
Heiser  inferred the annual sunflower subspecies, Helianthus annuus texanus, to be a stabilized hybrid resulting from the introgression of a small number of Helianthus debilis genes into a predominately H. a. annuus genome. Kim and Rieseberg  demonstrated that the introgression of only three small H. debilis genomicregions (containing three morphological quantitative trait loci (QTLs)) was sufficient to recapitulate the H. a. texanus phenotype (see  for a discussion of the parameters of QTL analyses). This unique phenotype includes a combination of traits gained apparently from either H. a. annuus (for example, the shape of bracts surrounding the flower head and the shape of the fruits) or H. debilis (for example, stem speckling and fruit size) [6, 7]. Significantly, Whitney et al.  presented evidence that the introgression of H. debilis genomic material into a H. a. annuus genetic background not only accounted for the unique morphology of H. a. texanus, but also resulted in adaptive introgression. Specifically, the increased herbivore resistance of H. debilis was transferred into BC1 hybrids towards H. a. annuus.
Number and fraction of Iris fulva, Iris brevicaulis and their hybrids that survived an extended flooding event
Evidence for adaptive introgression in animals
Surveys of numerous loci across natural hybrid zones between the mouse species Mus musculus and Mus domesticus have been made. The detail obtained by applying a genomics approach to natural populations has allowed tests for deviations from neutral introgression - reflecting both positive and negative selection [10, 11]. Payseur et al.  detected X-chromosome loci that were apparently prevented from introgressing across a zone of hybridization between the two mouse species in southern Germany and western Austria. The lack of penetration was hypothesized to mark genomic regions contributing to the partial reproductive isolation between M. musculus and M. domesticus, as caused by selection against hybrids containing an admixture of heterospecific loci (that is, loci from the other species) . In contrast, some X-chromosome alleles of M. domesticus were found at higher than expected frequencies in populations of mice on the M. musculus side of the hybrid zone. These loci suggested
"...the possibility that positive selection may act to drive the spread of alleles from one species on to the genomic background of the other species..." (that is, reflecting adaptive trait introgression ). Selection can thus act in different 'directions' (either positively or negatively) on different portions of the genomes of hybrids. This differential selection results in introgression being favored or disfavored, depending upon the traits generated from the loci contained in the various genomic regions.
Loci distributed across the Mus autosomes also exhibited patterns of differential introgression. For example, Teeter et al.  reported restricted introgression for numerous loci, indicative of epistatic interactions contributing to lower hybrid fitness. These 'reproductive isolation' loci included genes that affect reproductive characteristics and responses to environmental cues . Although there was evidence for selection against the introgression of certain genomic regions, patterns of genetic variation also identified regions of high-frequency introgression. Consistent with previous findings for the X-chromosome loci , most of the introgression involved the occurrence of alleles from M. domesticus in a largely M. musculus genetic background . These loci included genes that underlie cell signaling, olfaction and response to pheromones, and are thus good candidates for adaptive introgression.
As discussed above, and by previous authors [1–3], both deterministic and stochastic factors will affect the evolutionary and ecological trajectories of hybrid popula tions. In particular, it has been suggested that selection against hybrids balanced by continual hybridization between the interacting taxa will play the major role in hybrid zone evolution . In contrast, others have argued for a differential selective coefficient depending upon which portions of the genomes of the hybridizing taxa are examined [1–4, 7–11]. In that conceptual framework, the genomes of hybridizing organisms would reflect the combined action of negative selection, positive selection and neutral diffusion of alleles from the alternative taxon. The genomes of organisms affected by differential introgression would thus be mosaics, possessing some cassettes of genomic material from the 'foreign' evolutionary lineage while retaining large stretches of non-introgressed genomic material [1–3].
Determining the evolutionary forces, whether stochastic or deterministic, that resulted in the introgression (or lack thereof) of foreign DNA is a primary question for students of natural hybridization. In this regard, the findings for Helianthus, Iris, Mus and Ambystoma indicate that models of evolutionary change remain inadequate when they neglect the role of divergence in the face of gene flow. When the process of introgression is one of the factors tested for in evolutionary analyses, it is often found. This genetic transfer, as reflected by genomes with an admixture of components from various lineages, is almost certainly indicative of the role of both stochastic and deterministic processes. Furthermore, unlike previous conclusions drawn when data were lacking (see  for a discussion of this debate), it is now apparent that the deterministic portion of the equation includes selection favoring the introgression of some alleles and traits (see, for example, [7–11]).
NHM was supported by National Science Foundation grant DEB-0816905.
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