Hybrid Populations Selectively Filter Gene Introgression Between Species

Abstract

Hybrids have long been recognized as a potential pathway for gene flow between species that can have important consequences for evolution and conservation biology. However, few studies have demonstrated that genes from one species can introgress or invade another species over a broad geographic area. Using 35 genetically mapped restriction fragment length polymorphism (RFLP) markers of two species of cottonwoods (Populus fremontii x P. angustifolia) and their hybrids (n = 550 trees), we showed that the majority of the genome is prohibited from introgressing from one species into the other. However, this barrier was not absolute; Fremont cpDNA and mtDNA were found throughout the geographic range of narrowleaf cottonwood, and 20% of the nuclear markers of Fremont cottonwood introgressed varying distances (some over 100 km) into the recipient species' range. Rates of nuclear introgression were variable, but two nuclear markers introgressed as fast as the haploid, cytoplasmically inherited chloroplast and mitochondrial markers. Our genome-wide analysis provides evidence for positive, negative, and neutral effects of introgression. For example, we predict that DNA fragments that introgress through several generations of backcrossing will be small, because small fragments are less likely to contain deleterious genes. These results argue that recombination will be important, that introgression can be very selective, and that evolutionary forces within the hybrid population to effectively "filter" gene flow between species. A strong filter may make introgression adaptive, prevent genetic assimilation, lead to relaxed isolating mechanisms, and contribute to the stability of hybrid zones. Thus, rather than hybridization being a negative factor as is commonly argued, natural hybridization between native species may provide important genetic variation that impacts both ecological and evolutionary processes. Finally, we propose two hypotheses that contrast the likelihood of contemporary versus ancient introgression in this system.

Recent, Allopatric, Homoploid Hybrid Speciation: The Origin of Senecio Squalidus (Asteraceae) in the British Isles From a Hybrid Zone on Mount Etna, Sicily

“…Assuming that the RAPD/ISSR markers examined are selectively neutral, the notable changes in frequency observed across the elevation gradient suggest that they are linked to loci subject to selection (Szymura and Barton 1991;Martinsen et al 2001). Concordance between clines for different markers implies that the hybrid zone is maintained by a balance between selection and dispersal (Barton and Hewitt 1985).…”

Molecular detection of hybridization between sympatric kangaroo species in south-eastern Australia

“…However, when speciation occurs allopatrically, reproductive isolation may remain incomplete, allowing hybridization and the subsequent introgression of genes to occur upon secondary contact (Dowling and Secor, 1997). Although the evolutionary consequences of hybridization can be deleterious, causing sterility or reduced fertility of offspring or resulting in a loss of genetic integrity and homogenization of gene pools (Rhymer and Simberloff, 1996), in some circumstances it may be beneficial by allowing the incorporation of novel genetic diversity and promoting adaptation to new environments or even speciation (Dowling and Secor, 1997;Martinsen et al, 2001;Salzburger et al, 2002;Smith et al, 2003). Although initially considered rare and usually deleterious among mammals, hybridization has been identified, to varying degrees, in various wild eutherian mammal taxa including cetaceans (Willis et al, 2004), seals (Lancaster et al, 2006;Kingston and Gwilliam, 2007), canids (Vila et al, 2003;Verardi et al, 2006), felids (Pierpaoli et al, 2003;Lecis et al, 2006), leporids (Thulin et al, 2006;MeloFerreira et al, 2007), martens (Kyle et al, 2003) and squirrels (Ermakov et al, 2006;Spiridonova et al, 2006).…”

Arthropod communities on hybrid and parental cottonwoods are phylogenetically structured by tree type: Implications for conservation of biodiversity in plant hybrid zones

“…However, molecular genetic data (Zinkgraf, 2012) show that backcrossed trees are indistinguishable from P. angustifolia , so we pooled data from backcrossed trees and P. angustifolia . The identity of individual hybrid trees was previously confirmed using RFLP data (Martinsen et al., 2001). …”