Eukaryote hybrid genomes

Abstract

Interspecific hybridization is the process where closely related species mate and produce offspring with admixed genomes. The genomic revolution has shown that hybridization is common, and that it may represent an important source of novel variation. Although most interspecific hybrids are sterile or less fit than their parents, some may survive and reproduce, enabling the transfer of adaptive variants across the species boundary, and even result in the formation of novel evolutionary lineages. There are two main variants of hybrid species genomes: allopolyploid, which have one full chromosome set from each parent species, and homoploid, which are a mosaic of the parent species genomes with no increase in chromosome number. The establishment of hybrid species requires the development of reproductive isolation against parental species. Allopolyploid species often have strong intrinsic reproductive barriers due to differences in chromosome number, and homoploid hybrids can become reproductively isolated from the parent species through assortment of genetic incompatibilities. However, both types of hybrids can become further reproductively isolated, gaining extrinsic isolation barriers, by exploiting novel ecological niches, relative to their parents. Hybrids represent the merging of divergent genomes and thus face problems arising from incompatible combinations of genes. Thus hybrid genomes are highly dynamic and undergo rapid evolutionary change, including genome stabilization in which selection against incompatible combinations results in fixation of compatible ancestry block combinations within the hybrid species. The potential for rapid adaptation or speciation makes hybrid genomes a particularly exciting subject of in evolutionary biology. Here we summarize how introgressed alleles or hybrid species can establish and how the resulting hybrid genomes evolve.

Fig 1. Potential evolutionary outcomes of hybridization.

While most hybridization events are evolutionary dead ends, hybridization may also lead to speciation reversal where two taxa merge into one or form a hybrid zone between parapatric taxa. Alternatively, only one species may disappear through genetic swamping if introgression is highly asymmetrical. When one or few heterospecific alleles are advantageous these can also introgress into one of the parent species’ genomes through repeated backcrossing. Hybrids may also form novel lineages that are reproductively isolated from both parent taxa. The coloured fractions of the bars in the bar plots below show the relative proportion of the genome belonging to the blue and green parental lineages respectively. The grey bars represent a speciation reversal where differences are selected against. Finally, if hybridization leads to unfit offspring, it may reduce the fitness of the involved parental taxa due to wasted reproductive effort and may increase extinction risks for these.

Fig 2. Schematic representation of homoploid and allopolyploid hybrid speciation.

As an example of a homoploid hybrid genome we present a schematic figure of the mosaic genome of the Italian sparrow which is a hybrid resulting from the anthropogenic house sparrow P. domesticus which spread across the Mediterranean with agriculture and encountered and hybridized with local populations of Spanish sparrow P. hispaniolensis [44,47,85]. As allopolyploid example we use the monkeyflower Mimulus peregrinus, an allohexaploid species that has evolved independently at least twice and which involves an intermediate, sexually-sterile but clonally vigorous F1 hybrid [115]. Sterile F1 hybrids have given rise to allopolyploids in other taxa (e.g. Spartina and Senecio), but allopolyploids can also form via fertile intermediate hybrids (e.g. Tragopogon).

Fig 3. The process of genome stabilization during hybrid speciation and introgression.

Both ecological selection pressures and selection to avoid intrinsic incompatibilities mould hybrid genomes. Depending on the balance between beneficial alleles and incompatibilities hybridisation can result either in an admixed taxon that is reproductively isolated from both parent taxa, or local introgression into a taxon that remains distinct in spite of occasional gene flow. RI abbreviates reproductive isolation. Fd is a measure of introgression and is estimated between a hybrid population and the red parent species, and the haplotypes illustrate example individuals in these populations.